Generally, studies have shown that, under demanding sensory conditions, A1 neuron responses and/or tuning are enhanced, consistent with findings across PSC modalities ( Gomez-Ramirez et al., 2016 Mineault et al., 2016 Carlson et al., 2018). However, decades of research confound categorization of A1 neurons as static sensory filters: myriad non-sensory variables affect firing rates (FRs), variance and noise correlations in A1 ( Osmanski and Wang, 2015 Angeloni and Geffen, 2018 David, 2018). Primary auditory cortex (A1) receives tonotopic feed-forward input from the lemniscal auditory thalamus and textbooks chiefly describe A1 concerning its role in spectral filtering ( Purves, 2004). Moreover, secondary and higher-order cortical neurons exhibit diminished, more complex, and task-dependent versions of these maps ( Rauschecker and Scott, 2009), and PFC neurons seem to represent all manner of stimulus and cognition-related variables without clear functional topography ( Machens et al., 2010). Numerous research has shown that PSC neurons form maps of the sensory epithelium, consistent with a role as low dimensional filters ( Merzenich et al., 1975). This account supports a feed-forward nervous system model, where information propagates along distinct processing stages, from peripheral sensory receptors to motor effectors, to enable perception and behavior ( Van Essen and Maunsell, 1983 Riesenhuber and Poggio, 1999). Accordingly, PSC neurons act as independent filters for low-dimensional sensory features ( Hubel and Wiesel, 1968 Merzenich et al., 1975 Kaas et al., 1979) while “association” and prefrontal cortical (PFC) neurons integrate information about behavioral demands and other sensory modalities ( Robinson et al., 1978). This dissociation of the effects of attention at the level of single neurons versus the population highlights the synergistic nature of cortical sound encoding and enriches our understanding of sensory cortical function.Ĭlassic accounts of primary sensory cortex (PSC) relegate PSC function to sensory filtering. However, when we pooled the activity of the sampled neurons via targeted dimensionality reduction (TDR), we found enhanced population-level representation of the attended feature and suppression of the distractor feature. Surprisingly, we found no average increase in responsiveness to, or encoding of, the attended feature across single neurons. We recorded from single neurons in monkey primary auditory cortex (A1), while subjects attended to either the spectral or temporal features of complex sounds.
SIGNIFICANCE STATEMENT The ability to adapt to a dynamic sensory environment promotes a range of important natural behaviors.
PRIMARY AUDITORY CORTEX CODE
These results suggest that an emergent population code not measurable at the single-neuron level might constitute the functional unit of sensory representation in PSC. Importantly, surrogate neural populations with intact single-neuron tuning but shuffled higher-order correlations among neurons fail to yield attention- related effects observed in the intact data. However, a population-level analysis reveals that ensembles of neurons exhibit enhanced encoding of attended sound features, and this population code tracks subjects' performance.
We found no overall enhancement of single-neuron coding of the attended feature, as attention could either diminish or enhance this coding. We found that single neurons tend to be high-dimensional, in that they exhibit substantial mixed selectivity for both sound features, as well as task context. Within a block, subjects attended to one feature of the sound in a selective change detection task. We presented sounds that varied along spectral and temporal feature dimensions (carrier bandwidth and temporal envelope, respectively). In order to illuminate how A1 supports flexible perception in rich acoustic environments, we recorded from A1 neurons while rhesus macaques (one male, one female) performed a feature-selective attention task. However, real-world stimuli usually vary along many feature dimensions and behavioral demands change constantly.
Typically, studies of PSC measure neurons' responses along few (one or two) stimulus and/or behavioral dimensions. Textbook descriptions of primary sensory cortex (PSC) revolve around single neurons' representation of low-dimensional sensory features, such as visual object orientation in primary visual cortex (V1), location of somatic touch in primary somatosensory cortex (S1), and sound frequency in primary auditory cortex (A1).
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