Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex

Abstract

We recorded from single neurons of the primary auditory cortex (A1), while trained monkeys reported a decision based on the comparison of 2 acoustic flutter stimuli. Crucially, to form the decision, monkeys had to compare the second stimulus rate to the memory trace of the first stimulus rate. We found that the responses of A1 neurons encode stimulus rates both through their periodicity and through their firing rates during the stimulation periods, but not during the working memory and decision components of this task. Neurometric thresholds based on firing rate were very similar to the monkey's discrimination thresholds, whereas neurometric thresholds based on periodicity were lower than the experimental thresholds. Thus, an observer could solve this task with a precision similar to that of the monkey based only on the firing rates evoked by the stimuli. These results suggest that the A1 is exclusively associated with the sensory and not with the cognitive components of this task.decision making ͉ monkeys ͉ working memory ͉ psychophysics ͉ neurophysiology T he problem of how sensory experiences arise from activity in the brain has stimulated a large amount of research in neuroscience (1, 2). A major component of this problem involves understanding how the brain represents sensory features-that is, what attributes of the neural responses evoked by a stimulus are meaningful for sensation, perception, memory, and decisionmaking? To confront these issues unambiguously, experimental methods should conform to 2 essential conditions: first, the sensory stimulus must be under precise, quantitative control, and second, the subject's psychophysical responses should be well controlled and quantitatively measured. Most experimental paradigms meeting these standards have involved vision (1, 3) and somatosensation (2, 4). In comparison, the amount of research about audition using this approach is scant (5). Most of the studies in the auditory cortex and related areas have described the response properties of neurons to auditory scenes in anesthetized and awake animals, and how these are affected by different task conditions (5-21). But how the neural representations of acoustic stimuli are related to perception, memory and decision making is not known.We addressed this problem by recording the activity of single neurons in the primary auditory cortex (A1), while trained monkeys discriminated the difference in rate of 2 acoustic flutter stimuli (range of 4-40 Hz). The sensation of acoustic flutter is produced by slow repetition of an acoustic stimulus (11). The rate of the acoustic flutter is determined by the interval between the acoustic stimuli (pulse trains). In the acoustic flutter discrimination task, monkeys report whether the second stimulus rate (f2) is higher or lower than the first stimulus rate (f1). This cognitive operation requires that subjects compare information of f2 with a stored trace of f1 to form a decision, that is, whether f2 Ͼ f1 or f2 Ͻ f1, and to report their perceptual evaluation after a short, fix...

Neural encoding of auditory discrimination in ventral premotor cortex

“…These results contrast with those obtained in primary auditory cortex (A1) during the same task (9). In that study, we found that A1 neurons responded exclusively during the stimulation periods, but not during the delay periods of the task.…”

“…1A) until their psychophysical thresholds were stable (9). We avoided the issue of task difficulty during the recordings by using a stimulus set that had large differences between f1 and f2 (Fig.…”

“…The contribution of sensory cortices in this cognitive operation has been investigated before, but the results suggest that they are primarily associated with stimulus encoding (4)(5)(6)(7)(8)(9). In contrast, those cortical areas that receive inputs from sensory and memory circuits, and send outputs to the motor circuits appear well suited for elaborating perceptual decisions (10)(11)(12)(13)(14)(15)(16).…”

“…The sensation of acoustic flutter is produced by slow repetitions of an acoustic stimulus. The rate of the acoustic flutter is determined by the interval between each pulse (each pulse lasts 20 ms at 1 KHz) in the stimulus trains (9). In the acoustic flutter discrimination task, monkeys report whether the second stimulus rate (f2) is higher or lower than the first stimulus rate (f1).…”

“…We addressed this problem by recording the activity of single neurons in VPC while trained monkeys discriminated the difference in rate of two acoustic flutter stimuli (range of 4-40 Hz) (9). The sensation of acoustic flutter is produced by slow repetitions of an acoustic stimulus.…”