Functional network properties of the auditory cortex

A fundamental goal of the auditory system is to parse an unlabeled mixture of environmental auditory stimuli into coherent perceptual units (Bregman, 1990). The auditory system accomplishes this task, in part, by computations that group together stimuli with similar spectral and temporal features, while simultaneously segregating stimuli with different spectral and temporal features into different groups. Groupings with similar spectral and temporal features lead to the generation of coherent auditory perceptual units, which are also known as auditory objects (Bizley and Cohen, 2013; Griffiths and Warren, 2004).

Our understanding of these stimulus-to-perception computations has been facilitated by elegant anatomical, psychophysical, electrophysiological, and imaging studies in humans and in non-human animal models. However, there are still substantial gaps in our understanding of the relationship between neural activity (in particular, spiking activity) in the auditory cortex, perception, and behavior (Banno et al., 2020; Cohen, 2012). Here, we discuss and review two gaps in our understanding: (1) the specific and differential contributions of different fields of the auditory cortex to auditory perception and behavior and (2) the way network activity impact and facilitate auditory information processing. In particular, we emphasize recent work that has identified underlying computational principles in the cortex of non-human primates and when appropriate we note studies from other animal models of hearing.

In the 1990s, Hackett, Romanski, Kaas, Rauschecker, and others (Hackett et al., 1998, 1999; Kaas and Hackett, 1998, 1999; Romanski and Goldman-Rakic, 2002; Romanski et al., 1999; Romanski et al., 2000) revolutionized our understanding of cortical anatomical connectivity as it relates to auditory processing. First, Hackett and Kaas demonstrated a new organizational principle for the auditory cortex; namely, a “core” that is surrounded by a “belt”, which, in turn, is surrounded by a “parabelt”. From those initial anatomical studies, two cortical processing streams were identified: the so-called “dorsal” and “ventral” pathways. Because these pathways were hypothesized to be analogous to the visual dorsal and ventral pathways (Ungerleider and Mishkin, 1982), it was thought that they contribute to auditory perception and spatial /audiomotor behaviors, respectively.

However, despite the elegance of these studies, we still do not have a coherent theory of how auditory and related cognitive information is processed within and across defined auditory fields. For example, what information is preferentially processed in the primary auditory cortex and how is this processing different from processing that occurs in other core auditory fields? Further, we do not have a good understanding of how information is transformed and represented across different cortical fields (e.g., from the core to the belt and ultimately to the prefrontal cortex). Finally, at a higher hierarchical level of processing, the unique functional role(s) of the auditory dorsal and ventral pathways still remains an active area of research (Rauschecker and Scott, 2009).

Although single-unit recordings have shed considerable light on the functional properties of the auditory cortex and the representation of stimulus-, task-, and cognitive-related variables in individual auditory fields (Cohen, 2012; Fritz et al., 2013; King et al., 2018; Recanzone, 2018; Recanzone and Sutter, 2008; Shamma et al., 2013; Shamma et al., 2011; Tsunada and Cohen, 2014; Wang and Walker, 2012), the cortex is not just composed of billions of individual neurons, but instead, it is composed of networks of interconnected neurons (Cohen and Kohn, 2011; Kohn et al., 2016; Semedo et al., 2020). These cortical networks operate over different computational scales: network ensembles exist within a single cortical field (e.g., the primary auditory cortex), across cortical fields (e.g., primary and non-primary auditory cortex), and across brain systems (e.g., the dorsal and ventral auditory pathways or the auditory and visual pathways) (Atencio and Schreiner, 2016; Bastos et al., 2012; Fries, 2009, 2015; See et al., 2018; See et al., 2021). These spatial scales include not only feedforward patterns of connectivity but also complex patterns of feedback connectivity (Banno et al., 2020). Indeed, the richness and extent of auditory feedback connectivity distinguishes it from other sensory systems, like the visual system (Brugge, 1992; Felleman and Van Essen, 1991; Kaas and Hackett, 2000). Across these spatial scales, we can also consider different temporal scales of neural activity, which range from single-neuron spiking activity to local-field potentials to neural oscillations. Unfortunately, our understanding of the contribution of network activity to auditory information processing is relatively nascent.

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