Separate Neural Systems Research Articles

Controlled recall of verbal material in temporal lobe epilepsy

This study used a guided process-dissociation procedure to examine the contribution of controlled and automatic uses of memory to a cued-recall task in 24 patients with unilateral temporal lobe epilepsy (TLE: 12 left-sided; 12 right-sided), and 12 neurotypical controls. In an inclusion task, participants attempted to complete three-letter word stems using previously studied words, in an exclusion task they aimed to avoid using studied words to complete stems. Patients with left TLE produced fewer target completions under inclusion conditions. Completion rates were not significantly different under exclusion conditions. Estimates derived from process dissociation calculations, confirmed that the cued-recall deficit in left TLE patients arose entirely from impairment in controlled memory processes. There were no group differences in the estimates of automatic processes. Recognition judgements of stems corresponding to studied words did not differ between the groups. Overall the results support the view that controlled and automatic memory processes are mediated by separable neural systems. Hippocampal and related structures within the left MTL are more important than corresponding right hemisphere structures for the controlled retrieval of verbal material. In contrast, the findings from this study do not suggest that the left and right temporal lobes make a differential contribution to automatic memory processing. The theoretical and clinical relevance of these findings are discussed.

Language switching in the bilingual brain: What’s next?

Recent work using functional neuroimaging with early bilinguals has found little evidence for separate neural systems for each language during picture naming (Hernandez, A. E., Dapretto, M., Mazziotta, J., & Bookheimer, S. (2001). Language switching and language representation in Spanish–English bilinguals: An fMRI study. Neuroimage, 14, 510–520). However, switching between languages in early bilinguals during picture naming shows increased activity in the Dorsolateral Prefrontal Cortex (DLPFC) suggesting the importance of maintaining goal related information in order to bias subsequent response selection (Braver, T. S., Barch, D. M., Kelley, W. M., Buckner, R. L., Cohen, N. J., Miezin, F. M., et al. (2001). Direct comparison of prefrontal cortex regions engaged by working and long-term memory tasks. Neuroimage, 14, 48–59; Cohen, J. D., Braver, T. S., & O’Reilly, R. C. (1996). A computational approach to prefrontal cortex, cognitive control and schizophrenia: Recent developments and current challenges. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 351, 1515–1527; O’Reilly, R. C., Braver, T. S., & Cohen, J. D. (1999). A biologically based computational model of working memory. In E. Akira Miyake, E. Priti Shah & et al. (Eds.), Models of working memory: Mechanisms of active maintenance and executive control. (pp. 375–411): New York, NY, USA). The current study set out to test early bilinguals using a picture naming paradigm. Results revealed increased activity in the DLPFC and the superior parietal lobule during language switching compared to naming of pictures in a single language. Increased activity was also observed between early learned first and second languages. The results from single language conditions revealed differences in areas devoted to language processing such as the Superior Temporal Gyrus. However, increased activity in brain areas devoted to memory, somatosensory processing and emotion were also observed. Taken together these results replicate previous studies on language switching. They also extend studies on the neural bases of bilingualism by suggesting that early bilinguals’ representation of the two languages may be mediated by neural systems not typically associated with language. The article ends by considering future directions in understanding the brain bases of language switching and single language processing in bilinguals.

Tsallis’ non-extensive free energy as a subjective value of an uncertain reward

Recent studies in neuroeconomics and econophysics revealed the importance of reward expectation in decision under uncertainty. Behavioral neuroeconomic studies have proposed that the unpredictability and the probability of an uncertain reward are distinctly encoded as entropy and a distorted probability weight, respectively, in the separate neural systems. However, previous behavioral economic and decision-theoretic models could not quantify reward-seeking and uncertainty aversion in a theoretically consistent manner. In this paper, we have: (i) proposed that generalized Helmholtz free energy in Tsallis’ non-extensive thermostatistics can be utilized to quantify a perceived value of an uncertain reward, and (ii) empirically examined the explanatory powers of the models. Future study directions in neuroeconomics and econophysics by utilizing the Tsallis’ free energy model are discussed.

Motivation for reward as a function of required effort: Dissociating the ‘liking’ from the ‘wanting’ system in humans

Recent studies investigating the neurobiology of reward motivation in animals have begun to deconstruct reward into separable neural systems involving the ‘liking’ of a reward (hedonic enjoyment of consumption) versus the ‘wanting’ of a reward (incentive salience to obtain reward). To date, however, it is unclear whether these systems are also separable in humans. We examined this question by manipulating the effort (clicking on a moving square) required for participants to obtain a reward (humorous versus non-humorous cartoon). Overall, as the required effort to view a humorous cartoon increased, participants were less likely to choose this reward. Moreover, individual differences in cartoon preference predicted cartoon choice at low levels of required effort, but not at high levels of required effort. These findings suggest that manipulating effort may be a valid method for dissociating the ‘liking’ from ‘wanting’ components of reward motivation in humans.

Brain activity during visual versus kinesthetic imagery: An fMRI study

Although there is ample evidence that motor imagery activates similar cerebral regions to those solicited during actual movements, it is still unknown whether visual (VI) and kinesthetic imagery (KI) recruit comparable or distinct neural networks. The present study was thus designed to identify, through functional magnetic resonance imaging at 3.0 Tesla in 13 skilled imagers, the cerebral structures implicated in VI and KI. Participants were scanned in a perceptual control condition and while physically executing or focusing during motor imagery on either the visual or kinesthetic components of an explicitly known sequence of finger movements. Subjects' imagery abilities were assessed using well-established psychological, chronometric, and new physiological measures from the autonomic nervous system. Compared with the perceptual condition, physical executing, VI, and KI resulted in overlapping (albeit non-identical) brain activations, including motor-related regions and the inferior and superior parietal lobules. By contrast, a divergent pattern of increased activity was observed when VI and KI were compared directly: VI activated predominantly the occipital regions and the superior parietal lobules, whereas KI yielded more activity in motor-associated structures and the inferior parietal lobule. These results suggest that VI and KI are mediated through separate neural systems, which contribute differently during processes of motor learning and neurological rehabilitation.

Infection, Incest, and Iniquity: Investigating the Neural Correlates of Disgust and Morality

Disgust, an emotion related to avoiding harmful substances, has been linked to moral judgments in many behavioral studies. However, the fact that participants report feelings of disgust when thinking about feces and a heinous crime does not necessarily indicate that the same mechanisms mediate these reactions. Humans might instead have separate neural and physiological systems guiding aversive behaviors and judgments across different domains. The present interdisciplinary study used functional magnetic resonance imaging (n = 50) and behavioral assessment to investigate the biological homology of pathogen-related and moral disgust. We provide evidence that pathogen-related and sociomoral acts entrain many common as well as unique brain networks. We also investigated whether morality itself is composed of distinct neural and behavioral subdomains. We provide evidence that, despite their tendency to elicit similar ratings of moral wrongness, incestuous and nonsexual immoral acts entrain dramatically separate, while still overlapping, brain networks. These results (i) provide support for the view that the biological response of disgust is intimately tied to immorality, (ii) demonstrate that there are at least three separate domains of disgust, and (iii) suggest strongly that morality, like disgust, is not a unified psychological or neurological phenomenon.

Neural mechanisms supporting flexible performance adjustment during development

Feedback processing is crucial for successful performance adjustment following changing task demands. The present event-related fMRI study was aimed at investigating the developmental differences in brain regions associated with different aspects of feedback processing. Children age 8-11, adolescents age 14-15, and adults age 18-24 performed a rule switch task resembling the Wisconsin Card Sorting Task, and analyses focused on different types of negative and positive feedback. All age groups showed more activation in lateral orbitofrontal cortex (OFC), anterior cingulate cortex (ACC), dorsolateral prefrontal cortex (DLPFC), and superior parietal cortex following negative relative to positive performance feedback, but the regions contributed to different aspects of feedback processing and had separable developmental trajectories. OFC was adultlike by age 8-11, whereas parietal cortex was adultlike by age 14-15. DLPFC and ACC, in contrast, were still developing after age 14-15. These findings demonstrate that changes in separable neural systems underlie developmental differences in flexible performance adjustment. Supplementary data from this study are available online at the Psychonomic Society Archive of Norms, Stimuli, and Data, at www.psychonomic.org/archive.

Human brain activation during phonation and exhalation: Common volitional control for two upper airway functions

Phonation is defined as a laryngeal motor behavior used for speech production, which involves a highly specialized coordination of laryngeal and respiratory neuromuscular control. During speech, brief periods of vocal fold vibration for vowels are interspersed by voiced and unvoiced consonants, glottal stops and glottal fricatives (/h/). It remains unknown whether laryngeal/respiratory coordination of phonation for speech relies on separate neural systems from respiratory control or whether a common system controls both behaviors. To identify the central control system for human phonation, we used event-related fMRI to contrast brain activity during phonation with activity during prolonged exhalation in healthy adults. Both whole-brain analyses and region of interest comparisons were conducted. Production of syllables containing glottal stops and vowels was accompanied by activity in left sensorimotor, bilateral temporoparietal and medial motor areas. Prolonged exhalation similarly involved activity in left sensorimotor and temporoparietal areas but not medial motor areas. Significant differences between phonation and exhalation were found primarily in the bilateral auditory cortices with whole-brain analysis. The ROI analysis similarly indicated task differences in the auditory cortex with differences also detected in the inferolateral motor cortex and dentate nucleus of the cerebellum. A second experiment confirmed that activity in the auditory cortex only occurred during phonation for speech and did not depend upon sound production. Overall, a similar central neural system was identified for both speech phonation and voluntary exhalation that primarily differed in auditory monitoring.

Are There Separate Neural Systems for Spelling? New Insights into the Role of Rules and Memory in Spelling from Functional Magnetic Resonance Imaging

How do people spell the thousands of words at the tips of their tongues? Are words with regular sound-to-letter correspondences (e.g., "blink") spelled using the same neural systems as those with irregular correspondences (e.g., "yacht")? By offering novel neuroimaging evidence, we aim to advance contemporary debate about whether people use a single lexical memory process or whether dual mechanisms of lexical memory and sublexical phonological rules work in concert. We further aim to advance understanding of how people read by taking a fresh look at the related yet distinct capacity to spell. During functional magnetic resonance imaging scanning, 12 participants heard low-frequency regular words, irregular words, and nonwords (e.g., "shelm") and responded whether a visual presentation of the word was spelled correctly or incorrectly. While behavioral measures suggested some differences in accuracy and reaction time for the different word types, the neuroimaging results alone demonstrated robust differential processing and support a dual-route model of spelling, with implications for how spelling is taught and remediated in clinical and educational contexts.

Temporal Discounting Predicts Risk Sensitivity in Rhesus Macaques

Humans and animals tend both to avoid uncertainty and to prefer immediate over future rewards. The comorbidity of psychiatric disorders such as impulsivity, problem gambling, and addiction suggests that a common mechanism may underlie risk sensitivity and temporal discounting. Nonetheless, the precise relationship between these two traits remains largely unknown. To examine whether risk sensitivity and temporal discounting reflect a common process, we recorded choices made by two rhesus macaques in a visual gambling task while we varied the delay between trials. We found that preference for the risky option declined with increasing delay between sequential choices in the task, even when all other task parameters were held constant. These results were quantitatively predicted by a model that assumed that the subjective expected utility of the risky option is evaluated based on the expected time of the larger payoff. The importance of the larger payoff in this model suggests that the salience of larger payoffs played a critical role in determining the value of risky options. These data suggest that risk sensitivity may be a product of other cognitive processes, and specifically that myopia for the future and the salience of jackpots control the propensity to take a gamble.

Neural Correlates of Rule-Based and Information-Integration Visual Category Learning

An emerging theory of the neurobiology of category learning postulates that there are separate neural systems supporting the learning of categories based on verbalizeable rules (RB) or through implicit information integration (II). The medial temporal lobe (MTL) is thought to play a crucial role in successful RB categorization, whereas the posterior regions of the caudate are hypothesized to support II categorization. Functional neuroimaging was used to assess activity in these systems during category-learning tasks with category structures designed to afford either RB or II learning. Successful RB categorization was associated with relatively increased activity in the anterior MTL. Successful II categorization was associated with increased activity in the caudate body. The dissociation observed with neuroimaging is consistent with the roles of these systems in memory and dissociations reported in patient populations. Convergent evidence from these approaches consistently reinforces the idea of multiple neural systems supporting category learning.

The suprachiasmatic nucleus and sleep-wake regulation.

Human behavior is organized into 24-hour cycles that are typically composed of about 16 hours of wakefulness and about 8 hours of sleep. Sleep is an essential behavior and is critical for maintaining normal adaptive waking behavior. Both sleep and wake are initiated and maintained by separate and specific neural systems. The sleep-wake cycle is a function of 2 processes--a homeostatic drive for sleep that increases throughout the waking day and an opposing circadian influence that promotes wakefulness centered in the suprachiasmatic nucleus (SCN). A better understanding of the basis for sleep can help treatment and direct research about sleep.

Separate neural systems for processing action- or non-action-related sounds

The finding of a multisensory representation of actions in a premotor area of the monkey brain suggests that similar multimodal action-matching mechanisms may also be present in humans. Based on the existence of an audiovisual mirror system, we investigated whether sounds referring to actions that can be performed by the perceiver underlie different processing in the human brain. We recorded multichannel ERPs in a visuoauditory version of the repetition suppression paradigm to study the time course and the locus of the semantic processing of action-related sounds. Results show that the left posterior superior temporal and premotor areas are selectively modulated by action-related sounds; in contrast, the temporal pole is bilaterally modulated by non-action-related sounds. The present data, which support the hypothesis of distinctive action sound processing, may contribute to recent theories about the evolution of human language from a mirror system precursor.

Perception, Action, and Roelofs Effect: A Mere Illusion of Dissociation

A prominent and influential hypothesis of vision suggests the existence of two separate visual systems within the brain, one creating our perception of the world and another guiding our actions within it. The induced Roelofs effect has been described as providing strong evidence for this perception/action dissociation: When a small visual target is surrounded by a large frame positioned so that the frame's center is offset from the observer's midline, the perceived location of the target is shifted in the direction opposite the frame's offset. In spite of this perceptual mislocalization, however, the observer can accurately guide movements to the target location. Thus, perception is prone to the illusion while actions seem immune. Here we demonstrate that the Roelofs illusion is caused by a frame-induced transient distortion of the observer's apparent midline. We further demonstrate that actions guided to targets within this same distorted egocentric reference frame are fully expected to be accurate, since the errors of target localization will exactly cancel the errors of motor guidance. These findings provide a mechanistic explanation for the various perceptual and motor effects of the induced Roelofs illusion without requiring the existence of separate neural systems for perception and action. Given this, the behavioral dissociation that accompanies the Roelofs effect cannot be considered evidence of a dissociation of perception and action. This indicates a general need to re-evaluate the broad class of evidence purported to support this hypothesized dissociation.

Effects of lesions of the human posterior thalamus on ocular fixation during voluntary and visually triggered saccades

Objective: To investigate the role of the posterior thalamus in controlling voluntary and visually triggered eye movements and ocular fixation. Methods: The latency to initiate saccades to peripheral targets (visually...

Separate neural systems value immediate and delayed monetary rewards.

When humans are offered the choice between rewards available at different points in time, the relative values of the options are discounted according to their expected delays until delivery. Using functional magnetic resonance imaging, we examined the neural correlates of time discounting while subjects made a series of choices between monetary reward options that varied by delay to delivery. We demonstrate that two separate systems are involved in such decisions. Parts of the limbic system associated with the midbrain dopamine system, including paralimbic cortex, are preferentially activated by decisions involving immediately available rewards. In contrast, regions of the lateral prefrontal cortex and posterior parietal cortex are engaged uniformly by intertemporal choices irrespective of delay. Furthermore, the relative engagement of the two systems is directly associated with subjects' choices, with greater relative fronto-parietal activity when subjects choose longer term options.

Neural networks underlying endogenous and exogenous visual–spatial orienting

The orienting of visual-spatial attention is fundamental to most organisms and is controlled through external (exogenous) or internal (endogenous) processes. Exogenous orienting is considered to be reflexive and automatic, whereas endogenous orienting refers to the purposeful allocation of attentional resources to a predetermined location in space. Although behavioral, electrophysiological and lesion research in both primates and humans suggests that separate neural systems control these different modes of orienting, previous human neuroimaging studies have largely reported common neuronal substrates. Therefore, event-related FMRI (ER-FMRI) was used to independently examine different components of the orienting response including endogenous facilitation, exogenous facilitation and inhibition of return (IOR). In contrast to previous studies, endogenous versus exogenous facilitation resulted in widespread cortical activation including bilateral temporoparietal junction, bilateral superior temporal gyrus, right middle temporal gyrus, right frontal eye field and left intraparietal sulcus. Conversely, IOR compared to endogenous facilitation resulted in only a single focus of activation in the left superior temporal gyrus. These findings suggest that endogenous orienting activates a large cortical network to achieve internally generated shifts of attentional resources versus the automatic orienting that occurs with exogenous cues. However, similar networks may mediate endogenous orienting and IOR. The activation of the temporoparietal junction suggests that it is involved in more effortful processes, such as endogenous orienting, as well as in attentional reorienting and locating targets. Current results are discussed in terms of the functional development of the visual-spatial attentional system.

Shared and distinct neurophysiological components of the digits forward and backward tasks as revealed by functional neuroimaging

The digits forward (DF) and backward (DB) tasks are widely used neuropsychological measures believed to tap overlapping systems of phonological processing and working memory. Studies of focal brain lesions have partially elucidated the brain regions essential for these tasks; however relatively little information exists on the underlying functional neuroanatomy in the intact brain. We therefore examined the shared and separate neural systems of these tasks in two positron emission tomography (PET) experiments. In Experiment 1, eight healthy participants performed verbal DF, DB, and a sensorimotor control task during measurement of regional cerebral blood flow (rCBF). DF and DB each activated frontal, parietal, and cerebellar regions as well as prominently activating medial occipital cortex. To eliminate possible visuospatial confounds, Experiment 2 replicated the first experiment in six additional healthy participants who were blindfolded during the study. No differences in activation were found between the two experimental groups. Combined data from both experiments demonstrate that DF and DB rely upon a largely overlapping functional neural system associated with working memory, most notably right dorsolateral prefrontal cortex (DLPFC) and bilateral inferior parietal lobule (IPL) as well as the anterior cingulate, a region associated with attentional effort. The degree of activation increased linearly with increasing task difficulty in DF. DB additionally recruited bilateral DLPFC, left IPL, and Broca’s area. Medial occipital cortex (including higher and lower visual processing areas) was robustly activated in both DF and DB and could not be attributed to visual processing per se, suggesting a possible visual imagery strategy for these aural–verbal tasks.

Dissociating Explicit and Implicit Category Knowledge with fMRI

Neuroimaging of healthy volunteers identified separate neural systems supporting the expression of category knowledge depending on whether the learning mode was intentional or incidental. The same visual category was learned either intentionally or implicitly by two separate groupsof participants. During a categorization test, functional magnetic resonance imaging (fMRI) was used to compare brain activity evoked by category members and nonmembers. After implicit learning, when participants had learned the category incidentally, decreased occipital activity was observed for novel categorical stimuli compared with noncategorical stimuli. In contrast, after intentional learning, novel categorical stimuli evoked increased activity in the hippocampus, right prefrontal cortex, left inferior temporal cortex, precuneus, and posterior cingulate. Even though the categorization test was identical in the two conditions, the differences in brain activity indicate differing representations of category knowledge depending on whether the category had been learned intentionally or implicitly.

Grammatical processing of nouns and verbs in left frontal cortex?

We report the case of a brain-damaged subject R.C. who is more impaired at producing grammatical forms of words and pseudo-words used as verbs ( he judges, he wugs) than of the same words used as nouns ( the judges, the wugs). This pattern of performance constitutes the first clear demonstration that grammatical knowledge about verbs can be selectively impaired following brain damage. A comparison of R.C.’s behavioral and neurological profile with that of a patient who shows similar difficulties with nouns suggests that nouns and verbs are processed by separate neural systems with components in the left frontal lobe.