Learning strategy refinement reverses early sensory cortical map expansion but not behavior: Support for a theory of directed cortical substrates of learning and memory

Abstract

Primary sensory cortical fields develop highly specific associative representational plasticity, notably enlarged area of representation of reinforced signal stimuli within their topographic maps. However, overtraining subjects after they have solved an instrumental task can reduce or eliminate the expansion while the successful behavior remains. As the development of this plasticity depends on the learning strategy used to solve a task, we asked whether the loss of expansion is due to the strategy used during overtraining. Adult male rats were trained in a three-tone auditory discrimination task to bar-press to the CS+ for water reward and refrain from doing so during the CS− tones and silent intertrial intervals; errors were punished by a flashing light and time-out penalty. Groups acquired this task to a criterion within seven training sessions by relying on a strategy that was “bar-press from tone-onset-to-error signal” (“TOTE”). Three groups then received different levels of overtraining: Group ST, none; Group RT, one week; Group OT, three weeks. Post-training mapping of their primary auditory fields (A1) showed that Groups ST and RT had developed significantly expanded representational areas, specifically restricted to the frequency band of the CS+ tone. In contrast, the A1 of Group OT was no different from naïve controls. Analysis of learning strategy revealed this group had shifted strategy to a refinement of TOTE in which they self-terminated bar-presses before making an error (“iTOTE”). Across all animals, the greater the use of iTOTE, the smaller was the representation of the CS+ in A1. Thus, the loss of cortical expansion is attributable to a shift or refinement in strategy. This reversal of expansion was considered in light of a novel theoretical framework (CONCERTO) highlighting four basic principles of brain function that resolve anomalous findings and explaining why even a minor change in strategy would involve concomitant shifts of involved brain sites, including reversal of cortical expansion.

Cortical plasticity elicited by acoustically cued monetary losses: an ERP study

“…As suggested by theory, changes in the MMN amplitude induce the consolidation of memory traces and, therefore, functional cortical reorganisation 55 . Together with the aforementioned MMN findings of training-induced plasticity, the MMN results of our MID training fit a recently proposed systems-level theory of directed cortical plasticity 8 in learning and memory, which could induce the transient enlargement of the representational areas during the learning of behaviourally salient sounds followed by task-specific maintenance. In paradigms where sounds are used as conditioning stimuli, the training results in associative representational plasticity, which could facilitate responses to the cue stimuli 56 .…”

“…This and other examples of training-induced plasticity and adaptation to ecologically relevant stimuli are explained by the reorganisation of cortical representations in the human brain 1,2 . As shown by research with both animals 3 and human [4][5][6][7][8][9] , training-induced plasticity, sometimes referred to as directed cortical plasticity 8 , may lead to the transient reorganisation of cortical maps through the enlargement of a representation area, often followed by the subsequent reversal of cortical expansion in parallel with the establishment of interconnections among specific cortical and subcortical areas 10 . In the current study, we investigated whether repeated behaviour associated with monetary outcomes also modulates perceptual processing.…”

Silencing cortical activity during sound-localization training impairs auditory perceptual learning

“…Learning-related changes in the functional organization of A1 disappear with further training over time, even though improvements in behavioral performance are retained 36,45 . While they may still be manifest in A1 in other ways, such as via changes in dendritic spine dynamics 46,47 , it is also possible that the neural substrate for learned perceptual abilities, or in the case of our results a previously learned ability to reweight different spatial cues, lies elsewhere in the brain.…”

Recent advances in understanding the auditory cortex

“…Nevertheless, there have been few attempts to show that A1 plasticity is required for auditory perceptual learning. Indeed, training-induced changes in the functional organization of A1 have been found to disappear over time, even though improvements in behavioral performance are retained 159 , 160 . However, a recent study in which gerbils were trained on an amplitude-modulation detection task found both a close correlation between the magnitude and time course of cortical and behavioral plasticity and that inactivation of the auditory cortex reduced learning without affecting detection thresholds 161 .…”