Sharath Bennur

Distinct Representations of a Perceptual Decision and the Associated Oculomotor Plan in the Monkey Lateral Intraparietal Area

Perceptual decisions that are used to select particular actions can appear to be formed in an intentional framework, in which sensory evidence is converted directly into a plan to act. However, because the relationship between perceptual decision-making and action selection has been tested primarily under conditions in which the two could not be dissociated, it is not known whether this intentional framework plays a general role in forming perceptual decisions or only reflects certain task conditions. To dissociate decision and motor processing in the brain, we recorded from individual neurons in the lateral intraparietal area of monkeys performing a task that included a flexible association between a decision about the direction of random-dot motion and the direction of the appropriate eye-movement response. We targeted neurons that responded selectively in anticipation of a particular eye-movement response. We found that these neurons encoded the perceptual decision in a manner that was distinct from how they encoded the associated response. These decision-related signals were evident regardless of whether the appropriate decision–response association was indicated before, during, or after decision formation. The results suggest that perceptual decision-making and action selection are different brain processes that only appear to be inseparable under particular behavioral contexts.

The Relative Influences of Priors and Sensory Evidence on an Oculomotor Decision Variable During Perceptual Learning

Choice behavior on simple sensory-motor tasks can exhibit trial-to-trial dependencies. For perceptual tasks, these dependencies reflect the influence of prior trials on choices that are also guided by sensory evidence, which is often independent across trials. Here we show that the relative influences of prior trials and sensory evidence on choice behavior can be shaped by training, such that prior influences are strongest when perceptual sensitivity to the relevant sensory evidence is weakest and then decline steadily as sensitivity improves. We trained monkeys to decide the direction of random-dot motion and indicate their decision with an eye movement. We characterized sequential dependencies by relating current choices to weighted averages of prior choices. We then modeled behavior as a drift-diffusion process, in which the weighted average of prior choices provided an additive offset to a decision variable that integrated incoming motion evidence to govern choice. The average magnitude of offset within individual training sessions declined steadily as the quality of the integrated motion evidence increased over many months of training. The trial-by-trial magnitude of offset was correlated with signals related to developing commands that generate the oculomotor response but not with neural activity in either the middle temporal area, which represents information about the motion stimulus, or the lateral intraparietal area, which represents the sensory-motor conversion. The results suggest that training can shape the relative contributions of expectations based on prior trends and incoming sensory evidence to select and prepare visually guided actions.

Correlates of Perceptual Learning in an Oculomotor Decision Variable

In subjects trained extensively to indicate a perceptual decision with an action, neural commands that generate the action can represent the process of forming the decision. However, it is unknown whether this representation requires overtraining or reflects a more general link between perceptual and motor processing. We examined how perceptual processing is represented in motor commands in naive monkeys being trained on a demanding perceptual task, as they first establish the sensory–motor association and then learn to form more accurate perceptual judgments. The task required the monkeys to decide the direction of random-dot motion and respond with an eye movement to one of two visual targets. Using electrically evoked saccades, we examined oculomotor commands that developed during motion viewing. Throughout training, these commands tended to reflect both the subsequent binary choice of saccade target and the weighing of graded motion evidence used to arrive at that choice. Moreover, these decision-related oculomotor signals, along with the time needed to initiate the voluntary saccadic response, changed steadily as training progressed, approximately matching concomitant improvements in behavioral sensitivity to the motion stimulus. Thus, motor circuits may have general access to perceptual processing used to select between actions, even without extensive training. The results also suggest a novel candidate mechanism for some forms of perceptual learning, in which the brain learns rapidly to treat a perceptual decision as a problem of action selection and then over time to use sensory input more effectively to guide the selection process.

Biased Associative Representations in Parietal Cortex

Neurons in cortical sensory areas respond selectively to sensory stimuli, and the preferred stimulus typically varies among neurons so as to continuously span the sensory space. However, some neurons reflect sensory features that are learned or task dependent. For example, neurons in the lateral intraparietal area (LIP) reflect learned associations between visual stimuli. One might expect that roughly even numbers of LIP neurons would prefer each set of associated stimuli. However, in two associative learning experiments and a perceptual decision experiment, we found striking asymmetries: nearly all neurons recorded from an animal had a similar order of preference among associated stimuli. Behavioral factors could not account for these neuronal biases. A recent computational study proposed that population-firing patterns in parietal cortex have one-dimensional dynamics on long timescales, a possible consequence of recurrent connections that could drive persistent activity. One-dimensional dynamics would predict the biases in selectivity that we observed.

Recent refinements to cranial implants for rhesus macaques (Macaca mulatta).

The advent of cranial implants revolutionized primate neurophysiological research because they allow researchers to stably record neural activity from monkeys during active behavior. Cranial implants have improved over the years since their introduction, but chronic implants still increase the risk for medical complications including bacterial contamination and resultant infection, chronic inflammation, bone and tissue loss and complications related to the use of dental acrylic. These complications can lead to implant failure and early termination of study protocols. In an effort to reduce complications, we describe several refinements that have helped us improve cranial implants and the wellbeing of implanted primates.

Right way neurons

The visual and vestibular systems encode different, but complementary, aspects of self motion. A study in this issue sheds light on how the brain combines cues from these disparate sources, which are encoded by single neurons in the monkey extrastriate visual cortex, to support the perception of heading direction.

Functional Organization of the Ventral Auditory Pathway

The fundamental problem in audition is determining the mechanisms required by the brain to transform an unlabelled mixture of auditory stimuli into coherent perceptual representations. This process is called auditory-scene analysis. The perceptual representations that result from auditory-scene analysis are formed through a complex interaction of perceptual grouping, attention, categorization and decision-making. Despite a great deal of scientific energy devoted to understanding these aspects of hearing, we still do not understand (1) how sound perception arises from neural activity and (2) the causal relationship between neural activity and sound perception. Here, we review the role of the “ventral” auditory pathway in sound perception. We hypothesize that, in the early parts of the auditory cortex, neural activity reflects the auditory properties of a stimulus. However, in latter parts of the auditory cortex, neurons encode the sensory evidence that forms an auditory decision and are causally involved in the decision process. Finally, in the prefrontal cortex, which receives input from the auditory cortex, neural activity reflects the actual perceptual decision. Together, these studies indicate that the ventral pathway contains hierarchical circuits that are specialized for auditory perception and scene analysis.

Neural correlates of hearing in noise in macaque auditory cortex

The perception of sound in a noisy environment is a critical function of the auditory system. Here, we describe results from our study into the link between neural activity in the auditory cortex and the hearing-in-noise tasks described above. We recorded neural activity from single neurons in the core auditory cortex (i.e., A1) while monkeys were participating in these tasks. Neural recordings were conducted with tetrodes, and the frequency of the target matched the best frequency of the recorded auditory neuron. We found that the relative intensity of the target tone in the presence of the noise masker significantly modulated the response of A1 neurons. In contrast, the presentation of the target sound alone did not elicit a significant response from A1 neurons. This suggests a task-relevant contextual modulation of A1 responses during hearing in noise. Additionally we found no correlation between the monkeys behavioral choices—as assessed by their responses on choice trials—and A1 activity. Our results suggest that the encoding of a sound of interest in the presence of a noise masker is an active process, providing new insights into the neural basis for hearing in noise in the auditory system.