Neural correlates of instrumental learning in primary auditory cortex

Abstract

In instrumental learning, Thorndike's law of effect states that stimulus-response relations are strengthened if they occur prior to positive reinforcement and weakened if they occur prior to negative reinforcement. In this study, we demonstrate that neural correlates of Thorndike's law may be observed in the primary auditory cortex, A1. Adult owl monkeys learned to discriminate tones higher than a standard frequency. Responses recorded from implanted microelectrodes initially exhibited broad spectral selectivity over a four-to-five octave range. With training, frequency discrimination thresholds changed from close to one octave to about 1/12 octave. Physiological recordings during the week in which the monkey came under behavioral control signaled by a drop in measured threshold had stronger responses to all frequencies. During the same week, A1 neural responses to target stimuli increased relative to standard and nontarget stimuli. This emergent difference in responsiveness persisted throughout the subsequent weeks of behavioral training. These data suggest that behavioral responses to stimuli modulate responsiveness in primary cortical areas.

Figure 1

Schematic drawing of a trial. A trial began with an orienting response, the animal breaking an infrared beam in front of its nose. Two to six standard tones were then repeated. After the tones changed to the target frequency, which was higher than the standard frequency, the animal could remove its head from the beam to receive a fruit-juice reward.

Figure 2

(A) (Upper) The sum of all responses sampled from the array as a function of frequency and intensity in the first week of behavioral training. (Lower) Responses in the last week. The black bars indicate the range of frequencies and intensities used as targets in the behavior. (Left) Animal one; (Right) animal two. (B) The sum of all responses to different frequencies at the trained intensity. At the end of training, every standard frequency response was lower than the response to at least 10 of the next 12 higher frequencies. Each of the eight plots is individually normalized to its maximum and minimum response. Standard frequencies are indicated by thin vertical lines.

Figure 3

Changes in threshold and selectivity with time. (A) Thresholds vs. time are shown on the top for animal one. Selectivity of target and nontarget ranges are shown on the bottom. (B) Animal two. Targets were presented in frequency ranges symbolized with a circle and star. Nontarget ranges are symbolized by an X. In all cases, significant differences emerged between the target and nontarget frequency ranges.

Figure 4

Daily changes across the breakpoint in animal two for the upper frequency range. Circles show average response to the target frequency range. Xs show the daily response to the standards. Stars show the responses to frequencies not used in the behavior. All physiological responses are derived immediately before the corresponding behavioral sessions. The animal first achieved performance above chance before day 0 recordings.