Emergent Selectivity for Task-Relevant Stimuli in Higher-Order Auditory Cortex

Abstract

A variety of attention-related effects have been demonstrated in primary auditory cortex (A1). However, an understanding of the functional role of higher auditory cortical areas in guiding attention to acoustic stimuli has been elusive. We recorded from neurons in two tonotopic cortical belt areas in the dorsal posterior ectosylvian gyrus (dPEG) of ferrets trained on a simple auditory discrimination task. Neurons in dPEG showed similar basic auditory tuning properties to A1, but during behavior we observed marked differences between these areas. In the belt areas, changes in neuronal firing rate and response dynamics greatly enhanced responses to target stimuli relative to distractors, allowing for greater attentional selection during active listening. Consistent with existing anatomical evidence, the pattern of sensory tuning and behavioral modulation in auditory belt cortex links the spectro-temporal representation of the whole acoustic scene in A1 to a more abstracted representation of task-relevant stimuli observed in frontal cortex.

Duration estimation entails predicting when

“…Second, duration-dependent neurons are seen throughout the auditory pathways across species and in particular as early as inferior colliculi (Aubie et al, 2012;Pérez-González et al, 2006): auditory cortex responses may reflect processed timing information early on in the subcortical nuclei notably in the TEST condition. In a third alternative, the receptive fields of auditory neurons as early as primary auditory cortex show plasticity as a function of attention and task demands (Atiani et al, 2014;Fritz et al, 2003), thereby internal predictions generated at higher levels can shape the auditory evoked responses observed here and could instantiate stimulus offset prediction. It also noteworthy that the midlatency auditory responses result from multiple cortical sources located in auditory (Liégeois-Chauvel et al, 1994;Yvert et al, 2001) and arguably frontal (Garcia-Rill et al, 2008;Weisser et al, 2001) cortices, which leaves open the possibility of topdown modulation of midlatency and notably ramping activities observed here.…”

Cortico‐cortical connectivity within ferret auditory cortex

“…Previous tracer studies in ferret revealed that these areas are innervated by the ventral division of the MGB (Pallas et al, 1990), and that multiple areas, predominantly on the PEG, but also on the AEG, receive connections from the MEG (Wallace and Bajwa, 1991; Pallas and Sur, 1993; Gao and Pallas, 1999). Since these studies were completed, we have gained a deeper understanding of the functional organization of the auditory cortex as assessed by responses to both simple (Kowalski et al, 1995; Nelken et al, 2004; Bizley et al, 2005, 2007a) and complex stimuli (Nelken et al, 2008; Bizley et al, 2009, 2013; Atiani et al, 2014), warranting a more comprehensive investigation of the connectivity within the auditory cortex. Our anatomical investigations support the idea that distinct anterior and posterior processing pathways exist and extend our understanding about the organization of the auditory cortex in the ferret, thus providing crucial information to facilitate cross‐species comparisons.…”

“…The presence of multiple auditory cortical areas on the ectosylvian gyrus (EG) of this species was first demonstrated by using 2‐deoxyglucose autoradiography (Wallace et al, 1997) and subsequently confirmed by using optical imaging of intrinsic signals (Nelken et al, 2004) and single‐unit recording (Kelly et al, 1986; Kelly and Judge, 1994; Kowalski et al, 1995; Bizley et al, 2005). Although most electrophysiological recording studies have focused on the primary auditory cortex (A1) (Phillips et al, 1988; Kowalski et al, 1996; Schnupp et al, 2001; Fritz et al, 2003; Rabinowitz et al, 2011; Keating et al, 2013), the nonprimary auditory fields in this species are now receiving increasing attention (Nelken et al, 2008; Bizley et al, 2009, 2010, 2013; Walker et al, 2011; Atiani et al, 2014). …”

Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

“…Training ferrets to engage in auditory-cued selective attention tasks can produce rapid changes in the spatiotemporal receptive fields of individual neurons in A1 that persist for hours (Fritz et al 2003). Similarly, during performance of an auditory discrimination task these neurons can be seen to temporarily alter their adaptation properties to enhance the differences in response between relevant stimuli (Atiani et al 2014;Shamma and Fritz 2014;Yin et al 2014). It remains unclear whether these comparatively brief changes during auditory tasks reflect longerterm plasticity that allows the circuit to operate in different taskspecific "modes," or if this short-term response plasticity is mechanistically related to that seen with longer-term remapping at all.…”