Prefrontal-inferotemporal interaction is not always necessary for reversal learning

Abstract

Prefrontal cortex (PFC) is thought to have a wide-ranging role in cognition, often described as executive function or behavioral inhibition. A specific example of such a role is the inhibition of representations in more posterior regions of cortex in a "top-down" manner, a function thought to be tested by reversal learning tasks. The direct action of PFC on posterior regions can be directly tested by disconnecting PFC from the region in question. We tested whether PFC directly inhibits visual object representations in inferotemporal cortex (IT) during reversal learning by studying the effect, in macaque monkeys, of disconnecting PFC from IT by crossed unilateral ablations. We tested two visual object reversal learning tasks, namely serial and concurrent reversal learning. We found that the disconnection severely impairs serial reversal learning but leaves concurrent reversal learning completely intact. Thus, PFC cannot be said to always have direct inhibitory control over visual object representations in reversal learning. Furthermore, our results cannot be explained by generalized theories of PFC function such as executive function and behavioral inhibition, because those theories do not make predictions that differentiate different forms of reversal learning. The results do, however, support our proposal, based on other experimental evidence from macaque monkeys, that PFC has a highly specific role in the representation of temporally complex events.

Figure 1.

Intended extents of the crossed unilateral ablations of prefrontal cortex (top row, light gray) and inferotemporal cortex (bottom row, dark gray) shown from medial, ventral, and lateral views. The shaded areas indicate the areas of intended removal. For detailed description, see Materials and Methods. CIN, Cingulate sulcus; ROS, rostral sulcus; LOS, lateral orbital sulcus; MOS, medial orbital sulcus; PS, principal sulcus; AS, arcuate sulcus; OTS, occipitotemporal sulcus; AMTS, anterior middle temporal sulcus; RS, rhinal sulcus; IOS, intraoccipital sulcus; STS, superior temporal sulcus; LS, lateral sulcus.

Figure 2.

Stimuli from the two experiments. a, Examples of stimuli and their changing reward contingencies in experiment 1. For additional detail, see Materials and Methods, Task Procedure, Experiment 1. Each box represents two stimuli comprising a trial, presented together on the screen. There were 10 such problems in the experiment, of which four examples are shown here. Above the stimuli, a + symbol refers to the stimulus that was rewarded in that trial, and a − symbol refers to stimulus that was not rewarded on that trial. The top line refers to the initial acquisition stage, whereas subsequent lines refer to stages R1 and R2. In each case, monkeys learned a stage to a criterion of 90% within a session before moving on to the next stage. b, Stimuli used in experiment 2. For details, see Materials and Methods, Task Procedures, Experiment 2. The two stimuli were the only stimuli used throughout the experiment. In any given session, one was rewarded and one was not. These contingencies reversed every time the monkey reached criterion on a session.

Figure 3.

Coronal sections of the actual and reconstructed lesions of monkeys in experiment 1. This figure should be viewed in landscape format, with the two columns marked A to the left of the page. When viewed in this way, the leftmost column shows actual sections at different anteroposterior levels taken from monkey A. In the adjacent column, the extent of the cortical removal is reconstructed and shown in red on cresyl violet-stained sections taken from a normal macaque brain. The remaining columns show similar sections and reconstructions for monkeys B and C. This method of displaying the histology better illustrates the size of the lesions, in particular the removed sulci that may not be obvious from the original sections because of collapse of overlying cortex. The numbers to the left indicate millimeters anterior to the interaural line (estimated from Paxinos et al., 2000).

Figure 4.

Coronal sections of the actual and reconstructed lesions of monkeys in experiment 2. This figure should be viewed in landscape format, with the two columns marked D to the left of the page. When viewed in this way, the leftmost column shows actual sections at different anteroposterior levels taken from monkey D. In the adjacent column, the extent of the cortical removal is reconstructed and shown in red on cresyl violet-stained sections taken from a normal macaque brain. The remaining columns show similar sections and reconstructions for monkeys E and F. This method of displaying the histology better illustrates the size of the lesions, in particular the removed sulci that may not be obvious from the original sections because of collapse of overlying cortex. The numbers to the left indicate millimeters anterior to the interaural line (estimated from Paxinos et al., 2000).

Figure 5.

Performance of the monkeys in experiments 1 and 2. a, Preoperative performance test in serial reversal learning, experiment 2. The graph shows the mean number of errors committed per trial for the first 40 trials after a reversal (trial 1 being the first trial in which the new reward contingencies are encountered) by the two groups, in a performance test that comprised the last 12 reversals completed before surgery. Performance of the two groups is very similar. b, Performance test after unilateral prefrontal ablations in serial reversal learning, experiment 2. This performance test comprised the 12 reversals completed after the initial surgery to ablate the prefrontal cortex unilaterally but before the second surgery on the opposite inferior temporal cortex. Performance of the two groups is very similar, suggesting that the unilateral prefrontal lesions had no effect on performance of the task. c, Performance test after disconnection of prefrontal from inferior temporal cortex in serial reversal learning, experiment 2. The graph is directly comparable with d, showing learning curves for the two groups measured in mean errors per trial, and plotted across the first 40 trials since the reversal. Because there is only one problem in this task, this is therefore equivalent to the trials per problem plotted in the adjacent graph (D). d, Performance of the two groups in experiment 1, concurrent reversal learning, after disconnection of prefrontal from inferior temporal cortex. The graph displays a learning curve for the two groups on stimuli that had reversed object reward contingencies relative to the previous stage, collapsed over stages R1 and R2. The performance is measured as the mean errors per trial for each group, plotted across the first 40 trials per problem since the reversal, in which trial 1 is the first trial in which the monkey encounters reversed contingencies on that problem. The consistent spike in performance after 20 trials exists because the reversal learning was performed over two sessions (see procedures in Materials and Methods), and hence the spike reflects a mild decrement at the start of the second session.

Figure 6.

Preoperative formation of a reversal learning set by all six monkeys in experiment 2. The graph shows the mean number of errors made by the six monkeys in reaching criterion at each of the minimum of 60 reversals learned before surgery. The characteristic improvement to a high and stable level of performance indicates the formation of a reversal learning set.