Thomas M. Talavage

Improved auditory cortex imaging using clustered volume acquisitions

The effects of the noise of echo‐planar functional magnetic resonance imaging on auditory cortex responses were compared for two methods of acquiring functional MR data. Responses observed with a distributed volume acquisition sequence were compared to those obtained with a clustered volume acquisition sequence. In the former case, slices from the volume were acquired at equal intervals within the repetition time, whereas the latter acquired all slices in rapid succession at the end of the imaging period. The clustered volume acquisition provides a period of quiet during which a stimulus may be presented uninterrupted and uncontaminated by the noise of echo‐planar imaging. Both sequences were implemented on a General Electric Signa imager retrofitted for echo‐planar imaging by Advanced NMR Systems, Inc. The sequences were used to acquire 60 images per slice of a fixed volume of cerebral cortex while subjects were presented an instrumental music stimulus in an On vs. Off paradigm. Data were acquired for both sequences using TR values of 2, 3, 4, 6 and 8 sec. The clustered volume acquisition sequence was found to yield greater measures of dynamic range (percent signal change, mean statistical power per unit imaging time) across the tested range of TR values. Observations of more consistent spatial extent of responses, greater mean signal changes, and higher and more consistent values of mean t‐statistic per unit imaging time demonstrate the efficacy of using a clustered volume acquisition for fMRI of auditory cortex. Hum. Brain Mapping 7:89–97, 1999.

Functionally-Detected Cognitive Impairment in High School Football Players without Clinically-Diagnosed Concussion

Head trauma and concussion in football players have recently received considerable media attention. Postmortem evidence suggests that accrual of damage to the brain may occur with repeated blows to the head, even when the individual blows fail to produce clinical symptoms. There is an urgent need for improved detection and characterization of head trauma to reduce future injury risk and promote development of new therapies. In this study we examined neurological performance and health in the presence of head collision events in high school football players, using longitudinal measures of collision events (the HIT(™) System), neurocognitive testing (ImPACT(™)), and functional magnetic resonance imaging MRI (fMRI). Longitudinal assessment (including baseline) was conducted in 11 young men (ages 15-19 years) participating on the varsity and junior varsity football teams at a single high school. We expected and observed subjects in two previously described categories: (1) no clinically-diagnosed concussion and no changes in neurological behavior, and (2) clinically-diagnosed concussion with changes in neurological behavior. Additionally, we observed players in a previously undiscovered third category, who exhibited no clinically-observed symptoms associated with concussion, but who demonstrated measurable neurocognitive (primarily visual working memory) and neurophysiological (altered activation in the dorsolateral prefrontal cortex [DLPFC]) impairments. This new category was associated with significantly higher numbers of head collision events to the top-front of the head, directly above the DLPFC. The discovery of this new category suggests that more players are suffering neurological injury than are currently being detected using traditional concussion-assessment tools. These individuals are unlikely to undergo clinical evaluation, and thus may continue to participate in football-related activities, even when changes in brain physiology (and potential brain damage) are present, which will increase the risk of future neurological injury.

Language dominance determined by whole brain functional MRI in patients with brain lesions

Background: Functional MRI (fMRI) is of potential value in determining hemisphere dominance for language in epileptic patients. Objective: To develop and validate an fMRI-based method of determining language dominance for patients with a wide range of potentially operable brain lesions in addition to epilepsy. Methods: Initially, a within-subjects design was used with 19 healthy volunteers (11 strongly right-handed, 8 left-handed) to determine the relative lateralizing usefulness of three different language tasks in fMRI. An automated, hemispheric analysis of laterality was used to analyze whole brain fMRI data sets. To evaluate the clinical usefulness of this method, we compared fMRI-determined laterality with laterality determined by Wada testing or electrocortical stimulation mapping, or both, in 23 consecutive patients undergoing presurgical evaluation of language dominance. Results: Only the verb generation task was reliably lateralizing. fMRI, using the verb generation task and an automated hemispheric analysis method, was concordant with invasive measures in 22 of 23 patients (12 Wada, 11 cortical stimulation). For the single patient who was discordant, in whom a tumor involved one-third of the left hemisphere, fMRI became concordant when the tumor and its reflection in the right hemisphere were excluded from laterality analysis. No significant negative correlation was obtained between lesion size and strength of laterality for the patients with lesions involving the dominant hemisphere. Conclusion: This fMRI method shows potential for evaluating language dominance in patients with a variety of brain lesions.

Imaging Subcortical Auditory Activity in Humans

There is a lack of physiological data pertaining to how listening humans process auditory information. Functional magnetic resonance imaging (fMRI) has provided some data for the auditory cortex in awake humans, but there is still a paucity of comparable data for subcortical auditory areas where the early stages of processing take place, as amply demonstrated by single‐unit studies in animals. It is unclear why fMRI has been unsuccessful in imaging auditory brain‐stem activity, but one problem may be cardiac‐related, pulsatile brain‐stem motion. To examine this, a method eliminating such motion (using cardiac gating) was applied to map sound‐related activity in the auditory cortices and inferior colliculi in the brain stem. Activation in both the colliculi and cortex became more discernible when gating was used. In contrast with the cortex, the improvement in the colliculi resulted from a reduction in signal variability, rather than from an increase in percent signal change. This reduction is consistent with the hypothesis that motion or pulsatile flow is a major factor in brain‐stem imaging. The way now seems clear to studying activity throughout the human auditory pathway in listening humans. Hum. Brain Mapping 6:33–41, 1998.

Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football

Concussion is a growing public health issue in the United States, and chronic traumatic encephalopathy (CTE) is the chief long-term concern linked to repeated concussions. Recently, attention has shifted toward subconcussive blows and the role they may play in the development of CTE. We recruited a cohort of high school football players for two seasons of observation. Acceleration sensors were placed in the helmets, and all contact activity was monitored. Pre-season computer-based neuropsychological tests and functional magnetic resonance imaging (fMRI) tests were also obtained in order to assess cognitive and neurophysiological health. In-season follow-up scans were then obtained both from individuals who had sustained a clinically-diagnosed concussion and those who had not. These changes were then related through stepwise regression to history of blows recorded throughout the football season up to the date of the scan. In addition to those subjects who had sustained a concussion, a substantial portion of our cohort who did not sustain concussions showed significant neurophysiological changes. Stepwise regression indicated significant relationships between the number of blows sustained by a subject and the ensuing neurophysiological change. Our findings reinforce the hypothesis that the effects of repetitive blows to the head are cumulative and that repeated exposure to subconcussive blows is connected to pathologically altered neurophysiology.

Hemispheric roles in the perception of speech prosody

Speech prosody is processed in neither a single region nor a specific hemisphere, but engages multiple areas comprising a large-scale spatially distributed network in both hemispheres. It remains to be elucidated whether hemispheric lateralization is based on higher-level prosodic representations or lower-level encoding of acoustic cues, or both. A cross-language (Chinese; English) fMRI study was conducted to examine brain activity elicited by selective attention to Chinese intonation (I) and tone (T) presented in three-syllable (I3, T3) and one-syllable (I1, T1) utterance pairs in a speeded response, discrimination paradigm. The Chinese group exhibited greater activity than the English in a left inferior parietal region across tasks (I1, I3, T1, T3). Only the Chinese group exhibited a leftward asymmetry in inferior parietal and posterior superior temporal (I1, I3, T1, T3), anterior temporal (I1, I3, T1, T3), and frontopolar (I1, I3) regions. Both language groups shared a rightward asymmetry in the mid portions of the superior temporal sulcus and middle frontal gyrus irrespective of prosodic unit or temporal interval. Hemispheric laterality effects enable us to distinguish brain activity associated with higher-order prosodic representations in the Chinese group from that associated with lower-level acoustic/auditory processes that are shared among listeners regardless of language experience. Lateralization is influenced by language experience that shapes the internal prosodic representation of an external auditory signal. We propose that speech prosody perception is mediated primarily by the RH, but is left-lateralized to task-dependent regions when language processing is required beyond the auditory analysis of the complex sound.

Modulation of auditory and visual cortex by selective attention is modality-dependent.

Using functional magnetic resonance imaging (fMRI), we investigated whether the response of auditory and visual cortex was modulated by attending selectively to either heard or seen numbers presented simultaneously. Alternating attention between modalities modulated fMRI signal within the corresponding sensory cortex. This study provides evidence that attention acts locally during early auditory cognitive sensory processing, and that modulation of auditory and visual sensory cortex by attention is modality-dependent.

Quantitative assessment of auditory cortex responses induced by imager acoustic noise

A clustered volume acquisition functional MRI pulse sequence was modified to assess the response to the acoustic noise of echo‐planar imaging in the auditory cortex and to determine whether it is possible to obtain data which is relatively free of acoustic contamination. The spatial location and strength (percent signal change) of cortical responses to the imager noise were examined by introducing extra gradient readouts, without slice excitation, to provide acoustic stimulation immediately prior to acquisition of a cerebral volume. The duration of acoustic stimulation was controlled by varying the number of extra gradient readouts. Slice acquisitions were clustered at the end of the repetition time (TR) period to prevent a response from being induced by the volume acquisition itself (“Intra‐Acquisition Response”). The cerebral volumes were acquired using a long TR in order to limit the integration of the cortical response across volume acquisitions (“Inter‐Acquisition Response”). Cortical responses were observed to be largest and most significant on the medial two‐thirds of Heschls gyrus, the location of primary auditory cortex. Mean signal changes induced by the imager noise were observed to be as high as 0.95%. A 2 sec delay prior to onset of the BOLD response was empirically determined. These results demonstrate that clustered volume acquisitions may be utilized for up to 2 sec of volume acquisition without inducing an appreciable Intra‐Acquisition Response and can be used, with a sufficiently long TR, to provide data which are similarly free of any Inter‐Acquisition Response. Hum. Brain Mapping 7:79–88, 1999.

Food-Related Odor Probes of Brain Reward Circuits During Hunger: A Pilot fMRI Study

Food aromas can be powerful appetitive cues in the natural environment. Although several studies have examined the cerebral responses to food images, none have used naturalistic food aromas to study obesity. Ten individuals (five normal‐weight and five obese) were recruited to undergo 24 h of food deprivation. Subjects were then imaged on a 3T Siemens Trio‐Tim scanner (Siemens, Erlangen, Germany) while smelling four food‐related odors (FRO; two sweet odors and two fat‐related) and four “nonappetitive odors” (NApO; e.g., Douglas fir). Before the imaging session, subjects rated their desire to eat each type of food to determine their most preferred (P‐FRO). Across all 10 subjects, P‐FRO elicited a greater blood oxygenation level dependent (BOLD) response than the NApO in limbic and reward‐related areas, including the bilateral insula and opercular (gustatory) cortex, the anterior and posterior cingulate, and ventral striatum. Obese subjects showed greater activation in the bilateral hippocampus/parahippocampal gyrus, but lean controls showed more activation in the posterior insula. Brain areas activated by food odors are similar to those elicited by cues of addictive substances, such as alcohol. Food odors are highly naturalistic stimuli, and may be effective probes of reward‐related networks in the context of hunger and obesity.

Alteration of default mode network in high school football athletes due to repetitive subconcussive mild traumatic brain injury: a resting-state functional magnetic resonance imaging study.

Long-term neurological damage as a result of head trauma while playing sports is a major concern for football athletes today. Repetitive concussions have been linked to many neurological disorders. Recently, it has been reported that repetitive subconcussive events can be a significant source of accrued damage. Since football athletes can experience hundreds of subconcussive hits during a single season, it is of utmost importance to understand their effect on brain health in the short and long term. In this study, resting-state functional magnetic resonance imaging (rs-fMRI) was used to study changes in the default mode network (DMN) after repetitive subconcussive mild traumatic brain injury. Twenty-two high school American football athletes, clinically asymptomatic, were scanned using the rs-fMRI for a single season. Baseline scans were acquired before the start of the season, and follow-up scans were obtained during and after the season to track the potential changes in the DMN as a result of experienced trauma. Ten noncollision-sport athletes were scanned over two sessions as controls. Overall, football athletes had significantly different functional connectivity measures than controls for most of the year. The presence of this deviation of football athletes from their healthy peers even before the start of the season suggests a neurological change that has accumulated over the years of playing the sport. Football athletes also demonstrate short-term changes relative to their own baseline at the start of the season. Football athletes exhibited hyperconnectivity in the DMN compared to controls for most of the sessions, which indicates that, despite the absence of symptoms typically associated with concussion, the repetitive trauma accrued produced long-term brain changes compared to their healthy peers.