Learning and attention increase visual response selectivity through distinct mechanisms

Abstract

Selectivity of cortical neurons for sensory stimuli can increase across days as animals learn their behavioral relevance, and across seconds when animals switch attention. While both phenomena are expressed in the same cortical circuit, it is unknown whether they rely on similar mechanisms. We imaged activity of the same neuronal populations in primary visual cortex as mice learned a visual discrimination task and subsequently performed an attention switching task. Selectivity changes due to learning and attention were uncorrelated in individual neurons. Selectivity increases after learning mainly arose from selective suppression of responses to one of the task relevant stimuli but from selective enhancement and suppression during attention. Learning and attention differentially affected interactions between excitatory and PV, SOM and VIP inhibitory cell classes. Circuit modelling revealed that cell class-specific top-down inputs best explained attentional modulation, while the reorganization of local functional connectivity accounted for learning related changes. Thus, distinct mechanisms underlie increased discriminability of relevant sensory stimuli across longer and shorter time scales.

Existing function in primary visual cortex is not perturbed by new skill acquisition of a non-matched sensory task

“…Similar to BCI training, a substantial fraction of V1 neurons retained their tuning preference after visual discrimination training, when probed outside of the training environment. It was previously observed that during a similar implementation of the visual discrimination task used here, activity during task execution was slightly depressed 50 , selectivity for the stimuli used during training increased in a context-dependent manner 16 , and selective suppression dominated when the animals were engaged in the task 51 . Our results are consistent with these previous observations, considering our measurements were made outside of the training environment and therefore can also be considered a different context.…”

“…The BCI task used in this study was multimodal in nature. To determine whether our results generalize to a single-modality task, we trained mice in a visual discrimination task in which it was previously established that V1 activity is required for improved behavioral performance 16,50,51 . Converging evidence indicates visual discrimination training enhances the neural representation of rewarded stimuli by increasing selectivity for the stimuli experienced during training 16,21 and in some cases improving response reliability 16 , and at the same time suppresses responses to non-relevant stimuli 16 .…”

Visuomotor association orthogonalizes visual cortical population codes

“…Furthermore, stimulus representations evolve as animals learn, even in primary sensory cortices. One might expect that after learning, the number of neurons selective for behaviorally-important stimuli increases, as has been observed in auditory (5,6), somatosensory (7,8), and visual cortex (9,10). Other studies, however, have found a paradoxical decrease in the number of cortical neurons responding optimally to learned stimuli (11,12), and in primary visual cortex (V1), neurons increase their slope at the task stimulus in a manner dependent on orientation preference (13).…”

Learning shapes cortical dynamics to enhance integration of relevant sensory input

“…Details of the experiment, data preprocessing, calculation of behavioral d-prime (Figure 3B), and fitting and validation of MVAR model on this dataset data have been described in detail in previous publications (Khan et al, 2018; see also Poort et al, 2015Poort et al, , 2021. Here, we summarize the MVAR model and provide details of novel MVAR analyses used in the present study.…”