International Journal of Psychophysiology 82 (2011) 16–23

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International Journal of Psychophysiology

Review

A history of sport-related concussion on event-related brain potential

a r t i c l e i n f o a b s t r a c t

Article history: Over the past decade, a growing body of research has detailed persistent changes to neuroelectric indices of
Received 20 October 2010 cognition in amateur and professional athletes with a concussion history. Here, we review the relevant
Received in revised form 7 February 2011 neuroelectric findings on this relationship while considering the duration from the last concussive event.
Accepted 11 February 2011
Collectively, the findings support a negative relation of concussive injury to neuroelectric indices of brain
Available online 19 February 2011
health and cognition in the presence of normal clinical findings. The results suggest that event-related brain
Keywords:
potentials are especially well-suited for identifying aspects of cognition that remain dysfunctional for an
Mild traumatic brain injury extended period of time, which are otherwise unidentified using standard neuropsychological tests. Such
N1 findings also suggest the need for additional research to fully elucidate the extent to which concussive injuries
P1 negatively impact brain health and cognition.
P3 © 2011 Elsevier B.V. All rights reserved.
ERN
Cognitive function
Athletes

1. Introduction and Hovda, 2001), with traditional thought suggesting no long term
effects to brain health and cognition. Indeed, several evaluations of
Sport-related concussion has been described by the Center for young adult athletes with a concussion history, who have progressed
Disease Control and Prevention as a ‘silent epidemic’ (Langlois et al., beyond the acute stages of injury, indicate normal performance on a
2004) with traditional estimates suggesting that 300,000 cases occur variety of clinical evaluations (Guskiewicz et al., 2002; Broglio et al.,
in a given year (Center for Disease Control, 1997). More recent injury 2006; Collie et al., 2006; Iverson et al., 2006). These evaluations were
estimates suggest that nearly 4 million injuries occur on an annual conducted using standard clinical tests designed to evaluate large
basis (Langlois et al., 2006), which now includes those injuries that do magnitude cognitive decrements associated with acute injury, the
not involve a loss of consciousness and those suspected to go sensitivity of which to detect persistent subtle changes in cognitive
unreported. Concussion is considered a type of mild traumatic brain functioning has been questioned (Broglio et al., 2006). Furthermore,
injury (mTBI) with an economic impact approaching $17 billion in recent evidence from former professional athletes suggests that
direct and indirect expenses annually (National Center for Injury cognitive health concerns emerge later in life in those with a
Prevention and Control, 2001). Injured individuals often display concussion history. Indeed, rates of depression (1.5 fold increase;
deficits in cognitive functioning, postural control, and increased Guskiewicz et al., 2007), mild cognitive impairment, dementia (5 fold
symptom reports (Broglio and Puetz, 2008) with known negative increase), and Alzheimer's disease (3 fold increase; Guskiewicz et al.,
effects on academic (Moser and Schatz, 2002; Covassin et al., 2003; 2005) are more common among ex-professional athletes and occur at
Moser et al., 2005) and job performance (Pelczar and Politynska, a younger age than in the general population. Thus, it is apparent that
1997). In most instances, injured individuals return to a pre-injury more sensitive measures of cognitive functioning are needed to
level of functioning on clinical evaluations within seven to ten days of accurately identify and evaluate the long term effects of concussion in
injury (McCrory et al., 2005), but the chronic effects of concussion previously injured individuals, who have not yet demonstrated
remain unclear. clinical pathologies.
As the acute signs and symptoms of concussion represent To this end, electroencephalography (EEG), and event-related
functional changes in brain, rather than structural damage (Giza brain potentials (ERPs) in particular, have demonstrated the requisite
sensitivity to better elucidate the existing literature gap between
normal-appearing clinical performance and covert clinical patholo-
⁎ Corresponding author at: Department of Kinesiology & Community Health, 331
Louise Freer Hall, 906 South Goodwin Avenue, University of Illinois, Urbana, IL 61801,
gies that might underlie subtle deficits in cognitive performance.
United States. Tel.: +1 217 244 1830; fax: +1 217 244 7322. Therefore, the primary purpose of this review is to synthesize the
E-mail address: broglio@illinois.edu (S.P. Broglio). current literature surrounding the persistent effects of concussion on

0167-8760/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.ijpsycho.2011.02.010
 S.P. Broglio et al. / International Journal of Psychophysiology 82 (2011) 16–23 17

long-term cognitive health as indexed by measures of the neuro- associated with attentional orienting (Knight, 1984; Kok, 2001;
electric system, with a secondary focus on the duration from injury. Rushby et al., 2005). Therefore, P3a amplitude is theorized to reflect
Although a body of literature investigating traumatic brain injuries greater focal attention toward the orientation of stimuli in the
(i.e., mild, moderate, and severe) occurring under other circum- environment (Polich, 2007). Accordingly, the P3a and P3b, along with
stances exists, this review is limited to those events occurring within a other ERP components, provide insight into select aspects of cognition
sporting context. In addition, papers addressing the long-term effects that may be altered by the persistent effects of concussion. Through
of sub-concussive forces (e.g., soccer heading and boxing) were also the use of these measures, inferences may be made regarding which
excluded due to a lack of standardization in diagnostic criteria. aspects of cognition continue to present dysfunction, and strategies
for cognitive interventions may be effectively formulated.
2. Event-related brain potentials
3. P3b
For almost a century, EEG has been extensively used to examine
electrical activity associated with normal and abnormal brain The initial work on the affect of sport-related concussion to ERP
function. More recently, ERPs have emerged as a technique to provide indices of cognitive dysfunction occurred approximately a decade ago
insight into the neural processes underlying perception, memory, and with three publications appearing from two different Canadian
action. ERPs refer to patterns of neuroelectric activation that occur in laboratories (Dupuis et al., 2000; Gaetz et al., 2000; Gaetz and
preparation for, or in response to, an event. ERPs may be obligatory Weinberg, 2000). Gaetz and Weinberg (2000) compared younger
responses (exogenous) to stimuli in the environment or reflect (18–34 years) and middle age (35–55 years) adults with a concussion
higher-order cognitive processes (endogenous) that often require history to those with no injury history. Participants underwent a
active consideration from the individual (Hugdahl et al., 1995). The battery of tests, including visual and auditory oddball tasks in which
benefit of the ERP approach lies in its temporal sensitivity, which ERPs were recorded. The results indicated that no differences existed
affords researchers the ability to parse the stimulus–response as a function of age grouping, but that 40% of the participants with a
relationship into its various component cognitive processes. That is, history of concussion fell more than 2.5 standard deviations outside
ERPs offer the requisite temporal resolution to determine which their normative database for the visual P3 (i.e., P3b), compared to 0%
aspects of the stimulus–response relationship are influenced by some in the non-concussed group (Gaetz and Weinberg, 2000). A similar,
manipulation, providing a greater understanding of the mechanisms yet smaller effect (10–20% above the 2.5 SD in the concussion history
underlying overt behavior. Further, the ERP technique has been used group based on age grouping) was observed for the auditory oddball
for many years, and is one of the most well studied Psychophysio- task. More traditional means of (statistically) analyzing the P3 data
logical techniques, producing a number of reliable and replicable indicated that the concussion history groups, regardless of age, had
components. However, ERPs have poor spatial resolution relative to smaller P3 amplitude and longer P3 latency relative to the group of
other neuroimaging techniques, making source localization difficult. individuals without a history of concussion (Gaetz and Weinberg,
Other criticisms of this approach include distortion of the signal due to 2000). These findings have been replicated in other laboratories as
the distance of the electrodes from the neuroelectric source, and the well (Gosselin et al., 2006). Based on contemporary theories of the P3
fact that ERPs can only be recorded from specific groups of neurons (Donchin and Coles, 1988; Polich, 2007), the findings suggest that a
with a specific orientation toward the scalp. Regardless of these history of concussion is related to deficits in attentional resource
shortcomings, ERP have remained a viable tool for investigating allocation in the service of context updating and delays in cognitive
covert aspects of human information processing, and have been used processing speed during stimulus acquisition.
to understand mTBI, even in the absence of clinical symptoms and However, other publications (Dupuis et al., 2000; Gaetz et al.,
overt cognitive deficits, which has quickly made them a valuable tool 2000) have provided only partial support for the P3 findings described
for the evaluation of sport-related concussion. above using similar oddball tasks. Dupuis et al. (2000) reported a
Although several components, such as the contingent negative decrease in P3 amplitude for previously concussed individuals who
variation (CNV), error-related negativity (ERN), and N2 have been had symptoms at the time of testing (1.7 ± 2 months post injury)
evaluated in relation to sport-related concussion, the P3 component compared to a group of previously concussed individuals who were
has captured considerable attention. Occurring about 300–800 ms asymptomatic at the time of testing (9.8 ± 7.8 months post injury)
following the presentation of a stimulus, the P3 (i.e., P300 of P3b) and non-concussed individuals. No group differences in P3 latency
component is thought to reflect neural activity associated with the were reported (Dupuis et al., 2000). Further, De Beaumont et al.
revision of the mental representation of the previous event (Donchin, (2007) reported smaller P3 amplitude for individuals with a history of
1981), such that the P3 is sensitive to the allocation of attentional multiple concussions relative to those with a single concussive event
resources during stimulus engagement (Polich, 2007). P3 timing, and those with no history of concussion. The data are especially
marked by its peak latency, is believed to index stimulus classification informative as they controlled for time since injury in their analyses,
and evaluation speed independent of response selection and action suggesting that the cumulative effects of multiple concussions on the
(Duncan-Johnson, 1981; Verleger, 1997). reduction in P3 amplitude are not merely functions of time since
The P3 has been further divided into the P3a and P3b subcompo- injury. Despite these lasting deficits in P3 amplitude, P3 latency
nents, which represent related but distinct neuroelectric processes differences were not observed between groups (De Beaumont et al.,
that are distinguished by their unique scalp distributions and the 2007).
context in which they occur (Polich, 2007). Stimulus discrimination Recently, Di Russo (Di Russo and Spinelli, 2010) evaluated
tasks, and in particular “oddball” paradigms, have been extensively executive control function in professional boxers, who had experi-
used to elicit these subcomponents. That is, the presentation of an enced at least one boxing loss by knockout (mean 3.1 knockouts),
infrequent target stimulus amid a train of frequent non-target stimuli indicating at least one concussion, albeit additional injuries may have
has been repeatedly demonstrated to elicit a pronounced P3b occurred. Professional fencers and non-athlete controls were
component, with a parietal scalp distribution (Polich, 2007). Con- recruited as controls, but concussion history was not reported.
versely, the infrequent presentation of an unexpected, uninstructed Participants executed a Go/No-Go task to evaluate the P3b response,
stimulus during a similar train of non-target stimuli has been wherein the boxers demonstrated suppressed amplitude and in-
observed to elicit a P3a component, marked by a fronto-central creased latency during the Go portion of the task compared to both
scalp distribution and a relatively short latency (Polich, 2007). The control groups. In addition, latency was increased relative to the
P3a is thought to reflect the selection of stimulus information controls during the No-Go portion of the task, which required
18 S.P. Broglio et al. / International Journal of Psychophysiology 82 (2011) 16–23

response inhibition for successful task performance. Collectively, et al., 2006) the ImPACT battery was not successful in discerning
these data suggest a decrease in the capacity to allocate attention prolonged cognitive dysfunction associated with concussion history.
resources, delays in processing contextual information, and poorer However, corroborating earlier P3b studies, a reduction in P3
capability to inhibit ‘pre-potent’ responses as a function of a history of amplitude was observed for those with a history of concussion
concussions and the sub-concussive blows that regularly occur during relative to those who had never sustained a brain injury. Interestingly,
boxing participation. However, the relationship between the number no such effect was observed for the P3a component, suggesting that
of concussions and neuroelectric indices of cognitive deficits was not while persistent cognitive dysfunction related to the allocation of
examined, indicating that this question remains open. attentional resources (i.e., P3b amplitude) remained more than three
Alternatively, Gaetz et al. (2000) compared four groups of years after injury, neuroelectric measures reflecting the attentional
participants who had either never sustained a concussion, or had a system, which governs orienting, were intact (Broglio et al., 2009).
history of 1, 2, or 3 or more concussions, and were at least six months Such a finding suggests selectivity in the prolonged effects of
removed from their last injury. They reported no group differences in concussion history on brain health and cognition in young adults.
P3 amplitude, but significantly longer P3 latency in the group with 3 However, other researchers have observed a different pattern of
or more concussions relative to the group who had never been injured findings, indicating a lack of consensus relative to the selectivity of
(Gaetz et al., 2000). No differences were observed for those who had concussion history on cognition. Specifically, De Beaumont et al. (2009)
sustained 1 or 2 concussions. Accordingly, findings across these examined concussion history in a group of older adults (M= 60.8 ±
studies are inconsistent, with some supporting a detrimental relation 5.2 years) who had sustained their last concussion approximately
of concussion history to cognitive processing speed (i.e., longer P3 30 years (Mage = 26.1± 9.2 years) prior to testing, and compared them
latencies), and others indicating reductions in attentional resource with a group of age-matched adults (M= 59.9 ± 9.1 years) who had
allocation (i.e., smaller P3 amplitude). It should be noted that all never been concussed. Participants performed neuropsychological tests,
studies had relatively small sample sizes and differences in the time followed by an auditory three stimulus oddball task. Results indicated
since the last concussive event differed across studies. Regardless, it is performance deficits on the neuropsychological tests and modified
clear that concussion has a lasting effect on the neuroelectric system flanker task in the concussion group, suggesting impaired memory and
that extends beyond the acute injury stage. inhibitory control. Importantly, the groups did not differ in their mental
Interestingly though, several reports have demonstrated a rela- status, as equivocal group differences were noted on the mini mental
tionship between self-reported symptoms and the P3 component. status exam. Further, concussed athletes demonstrated significantly
Specifically, Dupuis et al. (2000) indicated that participants in their smaller P3a and P3b amplitude, along with longer peak latencies for
symptomatic concussion group exhibited a negative correlation these components, relative to the no-injury history group (De Beaumont
between P3 amplitude and symptomatology. That is, those reporting et al., 2009). This pattern of findings suggests general deficits in
a higher number and greater severity of symptoms generated smaller cognitive function, given that deficits were observed for components of
P3 amplitude. No such relationship was observed for the number of cognition related to the allocation of attentional resources (P3b
concussions, severity of the most recent concussion, or time from the amplitude), the orienting of attention (P3a), cognitive processing
last injury (Dupuis et al., 2000). Parallel findings were reported by speed (P3 latency), as well as measures of cognitive control (response
Gosselin et al. (2006), who observed a negative relation between self- accuracy to neuropsychological battery).
reported headache and difficulty concentrating with P3 amplitude. Still other studies have observed deficits in P3a amplitude, without
Again, no such relationship was observed for the number of concomitant changes in latency (Theriault et al., 2009). Specifically,
concussions, the severity of the previous injuries, loss of conscious- asymptomatic athletes who had sustained multiple concussions were
ness, and the time from the previous concussive event (Gosselin et al., compared with athletes with no history of concussion. Concussed
2006). Further, Gaetz et al. (2000) reported a positive correlation athletes were further divided into groups based on those who had
between P3 latency and self-reported post-concussion symptoms of sustained their last concussion within the previous year and those
‘memory problems’ and ‘taking longer to think’. Similar findings were who had sustained their last concussion more than two years prior. In
reported by Lavoie et al. (2004) in which symptomatic athletes with a response to an auditory oddball task, recently concussed athletes (i.e.,
history of concussion had smaller P3 amplitudes than previously within the previous year) exhibited smaller P3a amplitude compared
concussed asymptomatic athletes and never concussed control to the non-concussed athletes. Those who had sustained their
athletes. Importantly, negative correlations were observed between concussion more than two years earlier demonstrated a non-
the severity of post concussion symptoms as well as the time since the significant trend for smaller P3a amplitude relative to non-concussed
last concussive event and P3 amplitude (Lavoie et al., 2004). athletes (Theriault et al., 2009). A similar effect was realized for P3b,
Collectively, these findings suggest that the P3 component may but it should be noted that component amplitudes were averaged
serve as an objective index for chronic cognitive dysfunction from overlapping electrodes (P3a: average of FCz, Cz, and CPz; and
associated with concussion history, with some evidence indicating P3b: average of Cz, CPz, and Pz), so the specificity of the two
that it may also reflect specific symptoms reported by the individual. components is unclear.
Future research clearly needs to advance these preliminary findings to Despite the interesting findings of these studies (De Beaumont
determine the nature and the extent of the relationship between the et al., 2009; Broglio et al., 2009; Theriault et al., 2009), conflicting
P3 component and prolonged symptoms experienced following a results were obtained, with the exception of P3b, indicating that a
concussive event. clear picture has not emerged relative to other aspects of cognition,
namely attentional orienting (as reflected by the P3a component). As
4. P3a such, this remains an open question in this literature. However, it is
also clear that multiple differences in experimental protocols and
Broglio et al. (2009) examined a history of sport-related study populations may have led to these conflicting outcomes.
concussion on the P3a and P3b components in a sample of 90 inter- Another possibility though, is that cognitive dysfunction related to
colligate club and recreational athletes (M = 19.7 ± 1.3 years), of attentional orienting may not be pronounced in young adults who
whom 46 had a prior history of concussion (3.4 years post-injury). have sustained a brain injury. But, over the course of the lifespan
Participants completed a standard sport specific neurocognitive such an injury may exacerbate cognitive declines associated with
assessment (i.e., ImPACT) and then performed a visual novelty normal aging resulting in clinical pathologies during later life. Where,
oddball task, while their ERPs were recorded. Similar to other on the other hand, processes subserving the allocation of atten-
previous reports (Broglio et al., 2006; Collie et al., 2006; Iverson tional resources are more profoundly affected by brain injury,
 S.P. Broglio et al. / International Journal of Psychophysiology 82 (2011) 16–23 19

demonstrating notable changes during earlier periods of the lifespan, toms at the time of testing. Symptomatic participants were an average
which remain dysfunctional later in life. of 15.1 (±16.6) weeks post injury, and asymptomatic participants
were an average of 5.3 (±3.1) weeks post injury (Gosselin et al.,
5. Sensory evoked potentials 2006). Participants' performance was equivalent on all neuropsycho-
logical tests, save for the digit symbol modalities test. Smaller N1
Exogenous (i.e., obligatory) evoked potentials such as the component amplitudes were observed for both symptomatic and
brainstem auditory evoked potential (BAEP), P1, and N1 reflect asymptomatic previously concussed participants in the unattended
automated sensory processing involved in the early stages of channel compared to the non-concussed group. This suggests that a
perception. The BAEP, first discovered by Jewett (1970), reflects history of concussion, regardless of the presence of symptoms, relates
basic neuronal function in the brainstem and peripheral nervous to persistent decrements in the encoding of basic auditory stimulus
system (Jewett and Williston, 1971). The P1 and N1 are closely related properties. Interestingly, the difference occurred in the unattended
exogenous components associated with sensory processing. The P1 is channel suggesting that concussion may lead to long-term decre-
thought to reflect sensory gating, preferential attention to sensory ments in the ability to process unattended sensory information.
inputs (Key et al., 2005), and the inhibition of irrelevant sensory Collectively, such a pattern of findings is difficult to interpret and
information (Waldo et al., 1992). The P1 also may reflect the process further study is needed to better elucidate potential differences in
of amplifying the signal to noise ratio in selective attention (Hillyard these sensory evoked potentials. However, the data provide some
and Muente, 1984; Hillyard and Anllo-Vento, 1998; Hillyard et al., preliminary evidence to suggest that sport-related concussions
1998) given that enhanced P1 amplitudes are observed in relation to deleteriously affect the speed at which middle age participants
attended stimuli (Awh et al., 2000). The N1 is an exogenous ERP encode basic stimulus features. That is, concussions experienced
component thought to reflect the discrimination and encoding of during younger adulthood may have a delayed onset of sensory
basic stimulus properties (Vogel and Luck, 2000). Similar to the P1, N1 dysfunction, or may be exacerbated during aging leading to the ability
amplitudes are enhanced in response to attended stimuli (Knight to detect such dysfunction later in the lifespan. Again, such
et al., 1981; Mangun, 1995; Awh et al., 2000) and may also reflect an speculation would require replication to draw this conclusion with
amplification of the signal to noise ratio during selective attention greater certainty.
processes (Hillyard and Muente, 1984; Hillyard and Anllo-Vento,
1998; Hillyard et al., 1998). 6. ERN
Among the earliest studies to examine ERP correlates of sport-
related concussion, Gaetz and Weinberg (2000) compared neurocog- The error-related negativity (ERN; also referred to as the Ne) is a
nitive function in previously concussed and non-concussed athletes response-locked ERP component that has recently been investigated
across multiple ages (see the P3b section above for details). The with considerable interest, (Falkenstein et al., 1991; Gehring et al.,
researchers used an extensive battery of tasks to elicit several ERP 1993; Scheffers et al., 1996; Luu et al., 2000; Ridderinkhof et al., 2002;
components. In particular, the BAEP was elicited by a click in the van Veen and Carter, 2002; Yeung et al., 2004). The ERN refers to a
stimulated ear and a white noise mask in the non-stimulated ear. The negative component that peaks approximately 80–100 ms after an
researchers used traditional statistical analyses as well as clinical, unintended response (Falkenstein et al., 2000; Holroyd and Coles,
qualitative criteria to evaluate their results. According to their clinical 2002), and neuroimaging research (Carter et al., 1998; Dehaene et al.,
criteria, 10% of concussed participants' aged 18–34 years had BAEP 1994; Miltner et al., 1997; van Veen and Carter, 2002) suggests that it
values beyond the normal range compared to 2.2% of their age- is generated in the dorsal anterior cingulate cortex. This component is
matched non-concussed peers. Interestingly, none of the participants' theorized to reflect action monitoring processes following the
aged 35–55 years in either the concussed or control groups had evaluation of erroneous behaviors to initiate top–down compensatory
abnormal BAEP values. Despite these descriptive clinical observations, processes, thus ensuring correct action on subsequent trials (Holroyd
traditional statistical analyses did not yield significant differences for and Coles, 2002; Yeung, 2004).
the BAEP component for younger or middle aged participants, Employing a modified flanker task to examine aspects of cognitive
suggesting that sport-related concussion does not detrimentally affect control, Pontifex et al. (2009) evaluated the ERN in individuals with a
basic auditory/brainstem processes. history of concussions (M = 1.7) and never before concussed
In addition to the BAEP, Gaetz and Weinberg (2000) evaluated participants. Concussed participants were an average of 2.9 years
participants' P1 component, which was elicited via a pattern reversal from their last concussive injury. Interestingly, concussed participants
paradigm (i.e., checkerboard). Again, researchers used both tradition- did not differ in behavioral task performance relative to control
al and clinical criteria to evaluate their results, with 30% of concussed participants on a neuropsychological test battery (i.e., ImPACT).
participants aged 18–34 years displaying abnormal P1 latencies, However, while performing the flanker task, participants with a
compared to none of their non-concussed peers. Similar to the history of concussion demonstrated significantly smaller ERN ampli-
younger concussed participants, 30% of the middle aged concussed tudes relative to those participants who had never sustained a
participants displayed abnormal P1 latencies compared to only 5% of concussion. This finding suggests that the ability to recognize errors or
control participants. Despite these descriptive clinical observations, evaluate response conflict is compromised in young adults with a
traditional experimental analyses again did not yield significant concussion history. Interestingly, Pearson correlations indicated a
differences for the P1 component for the younger participants. negative association between the number of concussive incidents and
However, middle aged concussed participants demonstrated signifi- the size of the ERN potential, with an increased number of injuries
cantly longer P1 latencies compared to their non-concussed peers, related to progressively smaller ERN amplitude (Pontifex et al., 2009).
suggesting that concussions experienced during younger adulthood Additionally, concussed participants evidenced decreased response
may lead to belabored sensory gating and preferential attention in accuracy and increased flanker interference relative to control
middle age (Gaetz and Weinberg, 2000). participants, suggesting decrements in the management of perceptual
In another experiment evaluating ERP correlates of sport-related and response interference. Taken together, these findings suggest that
concussion, Gosselin et al. (2006) compared the N1 component in both the ability to evaluate response conflict (i.e., error recognition)
previously concussed and never concussed athletes. Dichotic standard and the flexibly to adjust subsequent behavior are compromised in
and deviant tones were presented within the context of a modified individuals with a concussion history. Thus, neurocognitive decre-
auditory oddball task to elicit an ERP. Previously concussed partici- ments in cognitive control of action monitoring appear to endure for
pants were bifurcated according to the presence/absence of symp- several years after the last concussive incident. In addition, these data
20 S.P. Broglio et al. / International Journal of Psychophysiology 82 (2011) 16–23

further demonstrate the sensitivity of neuroelectric measurement to The inconsistent nature of concussive injuries suggests that the
detect subtle neurocognitive decrements in cognition that appear to impaired areas may not be limited to brain regions subserving
be linearly related to the number of previous injuries. cognitive function. Indeed, in the acute stage of injury several
investigations have indicated changes to postural control (Guskiewicz
7. Movement potentials et al., 2001; Guskiewicz et al., 1997). Thus, recording and evaluating
the neuroelectric system related to motor control may provide novel
The contingent negative variation (CNV) is an endogenous ERP insight into the long-term effects of injury. Motor-related cortical
component characterized by a large negative shift reflecting response potentials (MRCPs) are one such signal and are comprised of three
anticipation that occurs between a warning stimulus (S1) and an components: Bereitshafts potential, motor potentials, and motor
imperative stimulus (S2; Walter et al., 1964; Tecce, 1972; Tecce and monitoring potentials. Collectively, these signals are thought to
Cattanach, 1993; Bressler and Ding, 2006). The component has been represent cortical activity involved in the initiation and control of
further decomposed into two subcomponents: initial CNV (iCNV) and motor activity. Slobounov et al. (2002) have used a more compre-
terminal CNV (tCNV; Loveless and Sanford, 1974; Birbaumer et al., hensive ERP approach to examine the effects of concussion on
1990). The iCNV is the early portion of the component and has been movement. That is, they dissected the preparatory period prior to a
associated with the processing of information associated with the voluntary movement to examine differences in the Bereitshaftspoten-
warning stimulus, while the later occurring tCNV has been associated tial (BP), which has been found to reflect neural activation associated
with anticipation and response preparation for the imperative with the early stages of motor preparation. The negativity seen just
stimulus (Brunia, 1988; Rockstroh et al., 1993). prior to the onset of a movement, termed motor potentials (MP),
To date, only two studies have examined CNV correlates of sport- reflects neural activation associated with the later stages of motor
related concussion (Gaetz and Weinberg, 2000, Gaetz et al., 2000). preparation (Slobounov et al., 2002). Furthermore, the movement
Specifically, Gaetz and Weinberg (2000) compared neurocognitive monitoring potential (MMP), the slow negative potential thought to
function in previously concussed and non-concussed athletes across reflect the ongoing monitoring of persistent task-related movement,
multiple ages (see the P3b section above for more details) and used was also evaluated in six individuals with a history of a single sport-
visual and auditory stimulus pairings to elicit the CNV. Researchers related concussion, occurring 10–20 months previously (Slobounov
employed both clinical and statistical criteria to evaluate their results. et al., 2002). These findings were compared to those from six never-
The clinical results indicated that 40% of younger (18–34 years) before concussed individuals. All participants were asked to press a
concussed participants produced visual CNV responses beyond the load cell with their dominant index finger at 25% or 50% of their
normal range, as opposed to 10% of younger control participants. maximum voluntary contraction (MVC), such that force production
Further, statistical analyses revealed significant differences between would increase at a constant, gradual rate while visual feedback
younger concussed and control participants, suggesting that sport- regarding their current force level was provided.
related concussion negatively affected processes related to cueing, Slobounov et al. (2002) observed no group differences during the
motor anticipation, and response preparation in younger adults 25% MVC task. However, during the 50% MVC task, the concussed
(Gaetz and Weinberg, 2000). For middle aged (35–55 years) adults, group exhibited less negativity (i.e., smaller amplitude) across all
10% of concussed participants produced visual CNV responses beyond three movement potentials (i.e., BP, MP, and MMP) compared to the
the normal range, as opposed to 5% of control participants. Statistical non-concussed group. Further, whereas the non-concussed group had
analyses did not reveal any significant differences in CNV responses larger amplitude from the 25% to 50% MVC, no such increase was
for middle aged participants. Perhaps sport-related concussion observed for the concussed group, who failed to exhibit a BP during
negatively affects cueing, anticipation, and response preparation the 50% MVC (Slobounov et al., 2002). Behaviorally, deficits were also
processes in younger, but not middle aged adults (Gaetz and observed for the concussed group, with decreased accuracy during the
Weinberg, 2000). However, one consideration is that the mean time 50% MVC condition. The findings suggest that transient functional
from injury for the middle aged group was skewed by a single changes in neural networks underlying motor control and coordina-
participant, who was only one month post injury. With this exception tion are observed for a prolonged period following a concussive
removed, middle aged participants were significantly further from injury, with specific dysfunction related to the planning, initiation,
their last injury (42.4 vs. 37.2 months) than the young adult group. It and monitoring of voluntary movements (Slobounov et al., 2002). A
is possible that this period of time was sufficient for the resolution of follow-up study using a within-participants design corroborated
concussion effects on the CNV component, or perhaps concussion these deficits across the three motor potentials in concussed athletes
affects on motor processes are more difficult to detect in middle aged 3, 10, and 30 days post injury relative to baseline, indicating that
participants given that the CNV decreases with age (Dirnberger et al., dysfunction of motor control and coordination exists long after
2010; Gajewskia et al., 2010). Further study is necessary to fully clarify individuals are cleared to resume sport participation based on
the pattern of findings observed. standard neurocognitive assessments (Slobounov et al., 2005).
Examining CNV correlates of sport-related concussions, Gaetz et al.
(2000) compared the neurocognitive function of young athletes with 8. Conclusion
a history of 1, 2, or 3 or more concussions with control participants. All
participants were at least six months from their last injury, and The current review was intended to provide a description of
researchers used a visual stimulus pairing to elicit the CNV. Analyses previous works that utilized ERP measures to elucidate the persistent
failed to reveal any significant differences between concussed and effects of concussion on cognitive dysfunction. As noted throughout
non-concussed participants, regardless of the number of concussions, this review, a number of investigators have used the ERP approach
suggesting that a history of multiple concussions does not negatively because of its capacity to identify covert changes in cognitive
affect response preparation processes of young athletes (Gaetz et al., processes that occur in the time between stimulus engagement and
2000). Taken together, the implications of these findings remain response execution. That is, ERPs afford the opportunity to better
unclear, with one study suggesting that sport-related concussion may understand which aspects of cognition are affected by concussion due
negatively affect neuroelectric processes underlying young adult's to their superior temporal specificity relative to other neuroimaging
response preparation, and the other suggesting no such relationship. measures and overt behavioral responses elicited from clinical testing.
Thus, these findings should be interpreted cautiously, and further However, the ERP technique also has a number of shortcomings,
research is needed to better understand the relation of sport-related which may limit its feasibility for assessing sport-related concussion
concussion to processes subserving motor preparation. acutely. Specifically, EEG instrumentation is expensive and requires
 S.P. Broglio et al. / International Journal of Psychophysiology 82 (2011) 16–23 21

an individual with advanced training to not only collect data, but also processing speed (i.e., P3 latency), action monitoring (i.e., ERN), and
reduce and analyze the collected signal. Further, EEG preparation motor control and coordination (i.e., BP, MP, and MMP) in the
requires a significant amount of time, negating its use in the athletic presence of normal performance on a variety of clinical assessments.
environment where rapid decision making is often necessary. Given These prolonged changes suggest that concussed individuals do not
that ERPs reflect both exogenous and endogenous aspects of allocate the same level of attentional resources toward aspects of their
cognition, dedicated space that is void of extraneous stimuli is environment, nor are they capable of initiating and monitoring their
necessary to maximize signal quality. Such costs and space demands actions in a similar manner to those without a prior history of injury.
are not easily obtained in most sport settings. Alternatively, the EEG In addition, the changes brought about by concussion appear related
approach is better suited for return-to-play decision making and an to the number of concussions sustained by the individual and the time
examination of the persistent effects of concussion given its requisite from injury. That is, ERP deficits appear to increase in line with the
sensitivity in identifying deficits that otherwise go unnoticed using number of concussions sustained, while a reduction in deficits occurs
routine task performance measures. as the time from injury increases.
Regardless, the findings, summarized in Table 1, from multiple How these persistent changes in the neuroelectric system relate to
investigations suggest moderate to large decreases in ERP compo- the underlying pathophysiology of injury is not entirely clear. Animal
nents related to stimulus acquisition (e.g., P3 amplitude), cognitive models have demonstrated cerebral cell death within 72 h of mTBI

Table 1
Summary of published ERP and EE experiments. Effect sizes were calculated based on the values presented in the respective manuscripts as an estimate of concussion's impact on the
various indices of brain function.

Author Sample population Time from last injury Method Significant findings

Broglio et al. Intercollegiate and recreational athletes: m = 2.9 yrs Novelty oddball Concussed participants had smaller N2 (d = 2.89),
(2009) Concussed (m = 20 yrs; m = 1.7 P3a (d = 0.39), and P3b (d = 2.31) amplitudes
concussions); Controls (m = 19.4 yrs) compared to controls.
De Beaumont College football players: 1 concussion Visual search task Participants suffering multiple concussions
et al. (2007) Controls (m = 22.5 yrs); 1 concussion m = 4.7 yrs; demonstrated smaller P3 amplitudes than
(m = 23 yrs); 2+ concussions 2+ concussions participants with 1 concussion (d ≤ 2.71)
(m = 23.5 yrs, m = 2.8 concussions) m = 2.6 yrs
De Beaumont Concussed former athletes (m = 61 yrs), m = 34.7 yrs Auditory oddball Concussed participants had longer P3a latencies
et al. (2009) controls (m = 59 yrs). (d = 0.68) and amplitude (d = 0.39), and
P3b amplitudes (d = 0.52) compared to controls.
Di Russo and Professional boxers (n = 12, m = 28.1 yrs), n/a Go/No-Go Boxers demonstrated suppressed P3b amplitude
Spinelli (2010) professional fencers (n = 12, m = 26.3 yrs), (d ≤ 3.7) and increased latency (d ≤ 2.7)
student-controls (n = 12, m = 25.8 yrs) during the Go task and increased latency
(d ≤ 3.9) during the No-Go task
Dupuis et al. 3 groups of college athletes (m age = 21.5): Asymptomatic, Visual oddball Symptomatic participants demonstrated overall
(2000) control, asymptomatic and symptomatic. m = 9.75 months; smaller P3 amplitudes compared to asymptomatic
Symptomatic, and control participants (d = 1.02).
m = 1.7 months.
Gaetz and Contact Athletes divided into groups by Age 18–34 Visual oddball tasks: Concussed participants of all ages demonstrated
Weinberg age [18–34 (m = 25.5) and (m = 3.1 yrs); word, shape, and number; longer P3 latencies during all visual oddball
(2000) 35–55 (m = 42.4)] 35–55 Auditory oddball task tasks (d ≤ 7.68).
and compared to controls (m = 3.13 yrs)
Gaetz et al. (2000) High school Hockey players grouped by All subjects were Visual oddball task 3+ concussed participants demonstrated longer
number of concussion: 0, 1, 2, or 3+ N 6 months post- P3 latencies than control group (d = 1.21)
injury; 3+ group
m = 13.2 months
Gosselin et al. Professional, semi-professional and collegiate Asymptomatic, Auditory oddball Symptomatic athletes demonstrated smaller
(2006) hockey and football players: control m = 5.3 weeks; P2 amplitude (d = 0.74) than controls; greater
(m = 22.0 yrs);asymptomatic concussed Symptomatic, P3 amplitudes and longer P3 latencies were
(m = 26.1 yrs; m = 3.5 concussions); m = 15.1 weeks present in the concussed groups compared
and symptomatic concussed to the control group (d = n/a).
(m = 25.7 years; m = 5.1 concussions)
Lavoie et al. Student athletes (18–26 years) grouped into Asymptomatic Modified visual oddball Symptomatic participants demonstrated smaller
(2004) control, asymptomatic(m concussion = 2.6), (m = 9.9 months); P3 amplitude compared asymptomatic (d = 2.69)
and symptomatic (m concussion = 3.2) Symptomatic and controls (d = 1.72) participants
(m = 1.7 months)
Pontifex et al. Intercollegiate and recreational athletes: m = 2.9 yrs Modified flanker task ERN (Ne) on error trials was smaller for concussed
(2009) Concussed (m = 19.9 yrs; m = 1.7 participants compared to controls (d = 3.11).
concussions); Controls (m = 19.4 yrs)
Slobounov et al. Collegiate athletes: 10–20 months EEG during 25 and 50% Concussed athletes had significantly smaller
(2002) Concussed (m = 22.3 yrs) and maximum voluntary amplitudes during the 50% MVC for
Controls (n/a) contraction (MVC) of BP (d = 0.92 to 1.10), MP (d = 1.07 to 1.19)
the index finger and MMP (d = 1.10 to 1.22)
Slobounov et al. Collegiate athletes: Concussed (n/a) Evaluations at EEG taken during 3 static Significant differences (BP, MP, and MMP)
(2005) baseline and days and 1 dynamic posture between baseline and post-injury days (d = n/a)
3, 10, and 30
post-concussion.
Theriault et al. Varsity high school athletes: 3 groups: Recent concussion Auditory oddball Recent concussed participants displayed smaller P3a
(2009) Control (m = 22.1 yrs); Recent concussion m = 9.1 months; (d = 1.41) and P3b (d = 1.16) amplitudes compared
(m = 22.6 yrs; m = 2.9 concussions); Late concussion to controls. The Late concussion group displayed
Late concussion (m = 22.9 yrs; m = 33.2 months smaller P3a (d = 0.74) and P3b (d = 0.50) amplitudes
m = 2.5 concussions). compared to controls. Late concussion group
participants also displayed large P3b amplitudes
(d = 1.03), than those in the recent concussion group.

yrs = years: d = Cohen's d:, n/a = data unavailable.

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