Contribution of spiking activity in the primary auditory cortex to detection in noise.

A fundamental problem in hearing is detecting a "target" stimulus (e.g., a friend's voice) that is presented with a noisy background (e.g., the din of a crowded restaurant). Despite its importance to hearing, a relationship between spiking activity and behavioral performance during such a "detection-in-noise" task has yet to be fully elucidated. In this study, we recorded spiking activity in primary auditory cortex (A1) while rhesus monkeys detected a target stimulus that was presented with a noise background. Although some neurons were modulated, the response of the typical A1 neuron was not modulated by the stimulus- and task-related parameters of our task. In contrast, we found more robust representations of these parameters in population-level activity: small populations of neurons matched the monkeys' behavioral sensitivity. Overall, these findings are consistent with the hypothesis that the sensory evidence, which is needed to solve such detection-in-noise tasks, is represented in population-level A1 activity and may be available to be read out by downstream neurons that are involved in mediating this task.NEW & NOTEWORTHY This study examines the contribution of A1 to detecting a sound that is presented with a noisy background. We found that population-level A1 activity, but not single neurons, could provide the evidence needed to make this perceptual decision.

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.

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.

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.

Relationships between the threshold and slope of psychometric and neurometric functions during perceptual learning: implications for neuronal pooling.

Perceptual learning involves long-lasting improvements in the ability to perceive simple sensory stimuli. Some forms of perceptual learning are thought to involve an increasingly selective readout of sensory neurons that are most sensitive to the trained stimulus. Here we report novel changes in the relationship between the threshold and slope of the psychometric function during learning that are consistent with such changes in readout and can provide insights into the underlying neural mechanisms. In monkeys trained on a direction-discrimination task, perceptual improvements corresponded to lower psychometric thresholds and slightly shallower slopes. However, this relationship between threshold and slope was much weaker in comparable, ideal-observer "neurometric" functions of neurons in the middle temporal (MT) area, which represent sensory information used to perform the task and whose response properties did not change with training. We propose a linear/nonlinear pooling scheme to account for these results. According to this scheme, MT responses are pooled via linear weights that change with training to more selectively read out responses from the most sensitive neurons, thereby reducing predicted thresholds. An additional nonlinear (power-law) transformation does not change with training and causes the predicted psychometric function to become shallower as uninformative neurons are eliminated from the pooled signal. We show that this scheme is consistent with the measured changes in psychometric threshold and slope throughout training. The results suggest that some forms of perceptual learning involve improvements in a process akin to selective attention that pools the most informative neural signals to guide behavior.

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.

Stress enhances fear by forming new synapses with greater capacity for long-term potentiation in the amygdala.

Prolonged and severe stress leads to cognitive deficits, but facilitates emotional behaviour. Little is known about the synaptic basis for this contrast. Here, we report that in rats subjected to chronic immobilization stress, long-term potentiation (LTP) and NMDA receptor (NMDAR)-mediated synaptic responses are enhanced in principal neurons of the lateral amygdala, a brain area involved in fear memory formation. This is accompanied by electrophysiological and morphological changes consistent with the formation of 'silent synapses', containing only NMDARs. In parallel, chronic stress also reduces synaptic inhibition. Together, these synaptic changes would enable amygdalar neurons to undergo further experience-dependent modifications, leading to stronger fear memories. Consistent with this prediction, stressed animals exhibit enhanced conditioned fear. Hence, stress may leave its mark in the amygdala by generating new synapses with greater capacity for plasticity, thereby creating an ideal neuronal substrate for affective disorders. These findings also highlight the unique features of stress-induced plasticity in the amygdala that are strikingly different from the stress-induced impairment of structure and function in the hippocampus.

Natural variability in species-specific vocalizations constrains behavior and neural activity.

A listener's capacity to discriminate between sounds is related to the amount of acoustic variability that exists between these sounds. However, a full understanding of how this natural variability impacts neural activity and behavior is lacking. Here, we tested monkeys' ability to discriminate between different utterances of vocalizations from the same acoustic class (i.e., coos and grunts), while neural activity was simultaneously recorded in the anterolateral belt region (AL) of the auditory cortex, a brain region that is a part of a pathway that mediates auditory perception. Monkeys could discriminate between coos better than they could discriminate between grunts. We also found AL activity was more informative about different coos than different grunts. This difference could be attributed, in part, to our finding that coos had more acoustic variability than grunts. Thus, intrinsic acoustic variability constrained the discriminability of AL spike trains and the ability of rhesus monkeys to discriminate between vocalizations.

Understanding the neurophysiological basis of auditory abilities for social communication: a perspective on the value of ethological paradigms.

Acoustic communication between animals requires them to detect, discriminate, and categorize conspecific or heterospecific vocalizations in their natural environment. Laboratory studies of the auditory-processing abilities that facilitate these tasks have typically employed a broad range of acoustic stimuli, ranging from natural sounds like vocalizations to "artificial" sounds like pure tones and noise bursts. However, even when using vocalizations, laboratory studies often test abilities like categorization in relatively artificial contexts. Consequently, it is not clear whether neural and behavioral correlates of these tasks (1) reflect extensive operant training, which drives plastic changes in auditory pathways, or (2) the innate capacity of the animal and its auditory system. Here, we review a number of recent studies, which suggest that adopting more ethological paradigms utilizing natural communication contexts are scientifically important for elucidating how the auditory system normally processes and learns communication sounds. Additionally, since learning the meaning of communication sounds generally involves social interactions that engage neuromodulatory systems differently than laboratory-based conditioning paradigms, we argue that scientists need to pursue more ethological approaches to more fully inform our understanding of how the auditory system is engaged during acoustic communication. This article is part of a Special Issue entitled "Communication Sounds and the Brain: New Directions and Perspectives".

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.

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.