skip to main content


Title: Neural Interactions Underlying Visuomotor Associations in the Human Brain
Abstract

Rapid and flexible learning during behavioral choices is critical to our daily endeavors and constitutes a hallmark of dynamic reasoning. An important paradigm to examine flexible behavior involves learning new arbitrary associations mapping visual inputs to motor outputs. We conjectured that visuomotor rules are instantiated by translating visual signals into actions through dynamic interactions between visual, frontal and motor cortex. We evaluated the neural representation of such visuomotor rules by performing intracranial field potential recordings in epilepsy subjects during a rule-learning delayed match-to-behavior task. Learning new visuomotor mappings led to the emergence of specific responses associating visual signals with motor outputs in 3 anatomical clusters in frontal, anteroventral temporal and posterior parietal cortex. After learning, mapping selective signals during the delay period showed interactions with visual and motor signals. These observations provide initial steps towards elucidating the dynamic circuits underlying flexible behavior and how communication between subregions of frontal, temporal, and parietal cortex leads to rapid learning of task-relevant choices.

 
more » « less
NSF-PAR ID:
10127693
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Cerebral Cortex
Volume:
29
Issue:
11
ISSN:
1047-3211
Page Range / eLocation ID:
p. 4551-4567
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Learning and recognition can be improved by sorting novel items into categories and subcategories. Such hierarchical categorization is easy when it can be performed according to learned rules (e.g., “if car, then automatic or stick shift” or “if boat, then motor or sail”). Here, we present results showing that human participants acquire categorization rules for new visual hierarchies rapidly, and that, as they do, corresponding hierarchical representations of the categorized stimuli emerge in patterns of neural activation in the dorsal striatum and in posterior frontal and parietal cortex. Participants learned to categorize novel visual objects into a hierarchy with superordinate and subordinate levels based on the objects' shape features, without having been told the categorization rules for doing so. On each trial, participants were asked to report the category and subcategory of the object, after which they received feedback about the correctness of their categorization responses. Participants trained over the course of a one‐hour‐long session while their brain activation was measured using functional magnetic resonance imaging. Over the course of training, significant hierarchy learning took place as participants discovered the nested categorization rules, as evidenced by the occurrence of a learning trial, after which performance suddenly increased. This learning was associated with increased representational strength of the newly acquired hierarchical rules in a corticostriatal network including the posterior frontal and parietal cortex and the dorsal striatum. We also found evidence suggesting that reinforcement learning in the dorsal striatum contributed to hierarchical rule learning.

     
    more » « less
  2. Many goal-directed actions that require rapid visuomotor planning and perceptual decision-making are affected in older adults, causing difficulties in execution of many functional activities of daily living. Visuomotor planning and perceptual identification are mediated by the dorsal and ventral visual streams, respectively, but it is unclear how age-induced changes in sensory processing in these streams contribute to declines in visuomotor decision-making performance. Previously, we showed that in young adults, task demands influenced movement strategies during visuomotor decision-making, reflecting differential integration of sensory information between the two streams. Here, we asked the question if older adults would exhibit deficits in interactions between the two streams during demanding motor tasks. Older adults ( n = 15) and young controls ( n = 26) performed reaching or interception movements toward virtual objects. In some blocks of trials, participants also had to select an appropriate movement goal based on the shape of the object. Our results showed that older adults corrected fewer initial decision errors during both reaching and interception movements. During the interception decision task, older adults made more decision- and execution-related errors than young adults, which were related to early initiation of their movements. Together, these results suggest that older adults have a reduced ability to integrate new perceptual information to guide online action, which may reflect impaired ventral-dorsal stream interactions. NEW & NOTEWORTHY Older adults show declines in vision, decision-making, and motor control, which can lead to functional limitations. We used a rapid visuomotor decision task to examine how these deficits may interact to affect task performance. Compared with healthy young adults, older adults made more errors in both decision-making and motor execution, especially when the task required intercepting moving targets. This suggests that age-related declines in integrating perceptual and motor information may contribute to functional deficits. 
    more » « less
  3. The macaque middle temporal (MT) area is well known for its visual motion selectivity and relevance to motion perception, but the possibility of it also reflecting higher-level cognitive functions has largely been ignored. We tested for effects of task performance distinct from sensory encoding by manipulating subjects' temporal evidence-weighting strategy during a direction discrimination task while performing electrophysiological recordings from groups of MT neurons in rhesus macaques (one male, one female). This revealed multiple components of MT responses that were, surprisingly, not interpretable as behaviorally relevant modulations of motion encoding, or as bottom-up consequences of the readout of motion direction from MT. The time-varying motion-driven responses of MT were strongly affected by our strategic manipulation—but with time courses opposite the subjects' temporal weighting strategies. Furthermore, large choice-correlated signals were represented in population activity distinct from its motion responses, with multiple phases that lagged psychophysical readout and even continued after the stimulus (but which preceded motor responses). In summary, a novel experimental manipulation of strategy allowed us to control the time course of readout to challenge the correlation between sensory responses and choices, and population-level analyses of simultaneously recorded ensembles allowed us to identify strong signals that were so distinct from direction encoding that conventional, single-neuron-centric analyses could not have revealed or properly characterized them. Together, these approaches revealed multiple cognitive contributions to MT responses that are task related but not functionally relevant to encoding or decoding of motion for psychophysical direction discrimination, providing a new perspective on the assumed status of MT as a simple sensory area.

    SIGNIFICANCE STATEMENTThis study extends understanding of the middle temporal (MT) area beyond its representation of visual motion. Combining multineuron recordings, population-level analyses, and controlled manipulation of task strategy, we exposed signals that depended on changes in temporal weighting strategy, but did not manifest as feedforward effects on behavior. This was demonstrated by (1) an inverse relationship between temporal dynamics of behavioral readout and sensory encoding, (2) a choice-correlated signal that always lagged the stimulus time points most correlated with decisions, and (3) a distinct choice-correlated signal after the stimulus. These findings invite re-evaluation of MT for functions outside of its established sensory role and highlight the power of experimenter-controlled changes in temporal strategy, coupled with recording and analysis approaches that transcend the single-neuron perspective.

     
    more » « less
  4. Abstract

    Working memory (WM) is a capacity- and duration-limited system that forms a temporal bridge between fleeting sensory phenomena and possible actions. But how are the contents of WM used to guide behavior? A recent high-profile study reported evidence for simultaneous access to WM content and linked motor plans during WM-guided behavior, challenging serial models where task-relevant WM content is first selected and then mapped on to a task-relevant motor response. However, the task used in that study was not optimized to distinguish the selection of spatial versus nonspatial visual information stored in memory, nor to distinguish whether or how the chronometry of selecting nonspatial visual information stored in memory might differ from the selection of linked motor plans. Here, we revisited the chronometry of spatial, feature, and motor selection during WM-guided behavior using a task optimized to disentangle these processes. Concurrent EEG and eye position recordings revealed clear evidence for temporally dissociable spatial, feature, and motor selection during this task. Thus, our data reveal the existence of multiple WM selection mechanisms that belie conceptualizations of WM-guided behavior based on purely serial or parallel visuomotor processing.

     
    more » « less
  5. Abstract

    Modulation of vocal pitch is a key speech feature that conveys important linguistic and affective information. Auditory feedback is used to monitor and maintain pitch. We examined induced neural high gamma power (HGP) (65–150 Hz) using magnetoencephalography during pitch feedback control. Participants phonated into a microphone while hearing their auditory feedback through headphones. During each phonation, a single real‐time 400 ms pitch shift was applied to the auditory feedback. Participants compensated by rapidly changing their pitch to oppose the pitch shifts. This behavioral change required coordination of the neural speech motor control network, including integration of auditory and somatosensory feedback to initiate change in motor plans. We found increases in HGP across both hemispheres within 200 ms of pitch shifts, covering left sensory and right premotor, parietal, temporal, and frontal regions, involved in sensory detection and processing of the pitch shift. Later responses to pitch shifts (200–300 ms) were right dominant, in parietal, frontal, and temporal regions. Timing of activity in these regions indicates their role in coordinating motor change and detecting and processing of the sensory consequences of this change. Subtracting out cortical responses during passive listening to recordings of the phonations isolated HGP increases specific to speech production, highlighting right parietal and premotor cortex, and left posterior temporal cortex involvement in the motor response. Correlation of HGP with behavioral compensation demonstrated right frontal region involvement in modulating participant's compensatory response. This study highlights the bihemispheric sensorimotor cortical network involvement in auditory feedback‐based control of vocal pitch.Hum Brain Mapp 37:1474‐1485, 2016. © 2016 Wiley Periodicals, Inc.

     
    more » « less