We investigated the hypothesis that task performance can rapidly and adaptively reshape cortical receptive field properties in accord with specific task demands and salient sensory cues. We recorded neuronal responses in the primary auditory cortex of behaving ferrets that were trained to detect a target tone of any frequency. Cortical plasticity was quantified by measuring focal changes in each cell's spectrotemporal response field (STRF) in a series of passive and active behavioral conditions. STRF measurements were made simultaneously with task performance, providing multiple snapshots of the dynamic STRF during ongoing behavior. Attending to a specific target frequency during the detection task consistently induced localized facilitative changes in STRF shape, which were swift in onset. Such modulatory changes may enhance overall cortical responsiveness to the target tone and increase the likelihood of 'capturing' the attended target during the detection task. Some receptive field changes persisted for hours after the task was over and hence may contribute to long-term sensory memory.
'What' and 'where' visual streams define ventrolateral object and dorsolateral spatial processing domains in the prefrontal cortex of nonhuman primates. We looked for similar streams for auditory-prefrontal connections in rhesus macaques by combining microelectrode recording with anatomical tract-tracing. Injection of multiple tracers into physiologically mapped regions AL, ML and CL of the auditory belt cortex revealed that anterior belt cortex was reciprocally connected with the frontal pole (area 10), rostral principal sulcus (area 46) and ventral prefrontal regions (areas 12 and 45), whereas the caudal belt was mainly connected with the caudal principal sulcus (area 46) and frontal eye fields (area 8a). Thus separate auditory streams originate in caudal and rostral auditory cortex and target spatial and non-spatial domains of the frontal lobe, respectively.
As sensory stimuli and behavioral demands change, the attentive brain quickly identifies task-relevant stimuli and associates them with appropriate motor responses. The effects of attention on sensory processing vary across task paradigms, suggesting that the brain may use multiple strategies and mechanisms to highlight attended stimuli and link them to motor action. To better understand factors that contribute to these variable effects, we studied sensory representations in primary auditory cortex (A1) during two instrumental tasks that shared the same auditory discrimination but required different behavioral responses, either approach or avoidance. In the approach task, ferrets were rewarded for licking a spout when they heard a target tone amid a sequence of reference noise sounds. In the avoidance task, they were punished unless they inhibited licking to the target. To explore how these changes in task reward structure influenced attentiondriven rapid plasticity in A1, we measured changes in sensory neural responses during behavior. Responses to the target changed selectively during both tasks but did so with opposite sign. Despite the differences in sign, both effects were consistent with a general neural coding strategy that maximizes discriminability between sound classes. The dependence of the direction of plasticity on task suggests that representations in A1 change not only to sharpen representations of task-relevant stimuli but also to amplify responses to stimuli that signal aversive outcomes and lead to behavioral inhibition. Thus, top-down control of sensory processing can be shaped by task reward structure in addition to the required sensory discrimination.spectrotemporal receptive field | perception | grouping A s we interact with a world in flux, our brains adjust their responses to sensory stimuli, allowing us to meet changing behavioral demands (1, 2). Numerous studies have shown that attention contributes to this process by selectively modulating neural activity in brain areas that process sensory information, improving stimulus discriminability for grouping into task-relevant categories (3-13). However, the effects observed across behavioral paradigms are diverse, including changes in gain (4,5,7,14), selectivity (8,11,15,16), and functional connectivity (12), suggesting that the brain may use many possible strategies and mechanisms to highlight relevant stimuli and produce appropriate sensorimotor transformations. The specific effects of attention and other learned behaviors on representations, therefore, may depend not only on the required sensory grouping but also on a host of control signals reflecting task structure (17), motor responses (18, 19), associated reward (20), difficulty (21,22), and timing of decisions (23).To directly explore the influence of task structure on sensory representations, we recorded the activity of single neurons in primary auditory cortex (A1) during two different instrumental behaviors that required discrimination between the same two acoustic categories, pu...
Top-down signals from frontal cortex (FC) are conjectured to play a critical role in cognitive control of sensory processing. To explore this interaction, we compared activity in ferret FC and primary auditory cortex (A1) during auditory and visual tasks requiring discrimination between classes of reference and target stimuli. FC responses were behaviorally-gated, selectively encoded the timing and invariant behavioral meaning of target stimuli, could be rapid in onset, and sometimes persisted for hours following behavior. This mirrors earlier findings in A1that attention triggered rapid, selective, persistent, task-related changes in spectrotemporal receptive fields. Simultaneously recorded local field potentials (LFPs) revealed behaviorally-gated changes in inter-areal coherence, selectively modulated between FC and focal regions of A1 responsive to target sounds. These results suggest that A1 and FC dynamically establish a functional connection during auditory behavior that shapes the flow of sensory information and maintains a persistent trace of recent task-relevant stimulus features.
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