Dissociable influences of primary auditory cortex and the posterior auditory field on neuronal responses in the dorsal zone of auditory cortex

Abstract

Kok MA, Stolzberg D, Brown TA, Lomber SG. Dissociable influences of primary auditory cortex and the posterior auditory field on neuronal responses in the dorsal zone of auditory cortex. J Neurophysiol 113: 475-486, 2015. First published October 22, 2014 doi:10.1152/jn.00682.2014.-Current models of hierarchical processing in auditory cortex have been based principally on anatomical connectivity while functional interactions between individual regions have remained largely unexplored. Previous cortical deactivation studies in the cat have addressed functional reciprocal connectivity between primary auditory cortex (A1) and other hierarchically lower level fields. The present study sought to assess the functional contribution of inputs along multiple stages of the current hierarchical model to a higher order area, the dorsal zone (DZ) of auditory cortex, in the anaesthetized cat. Cryoloops were placed over A1 and posterior auditory field (PAF). Multiunit neuronal responses to noise burst and tonal stimuli were recorded in DZ during cortical deactivation of each field individually and in concert. Deactivation of A1 suppressed peak neuronal responses in DZ regardless of stimulus and resulted in increased minimum thresholds and reduced absolute bandwidths for tone frequency receptive fields in DZ. PAF deactivation had less robust effects on DZ firing rates and receptive fields compared with A1 deactivation, and combined A1/PAF cooling was largely driven by the effects of A1 deactivation at the population level. These results provide physiological support for the current anatomically based model of both serial and parallel processing schemes in auditory cortical hierarchical organization. auditory cortex; auditory pathways; hierarchy; reversible deactivation THE PAST TWO DECADES HAVE witnessed a dramatic increase in brain connectivity studies with advancements in functional imaging analysis methodology giving rise to the ability to noninvasively assess dependency effects between individual brain regions (Friston 2011). While a thorough understanding of the structural connectivity of the brain is a necessary component for understanding network function (Sporns 2012), investigations regarding the degree to which one brain region can exert influence on another are critical, as anatomical connectivity alone "is neither a sufficient nor a complete description of connectivity" (Friston 2011). Hierarchical processing schemes for cat auditory cortex have been proposed based mainly on structural connectivity analyses between individual regions of auditory cortex ( Fig. 1; Rouiller et al. 1991;Lee and Winer 2011), while the functional importance of these connections has remained largely unexplored. Using cortical cooling deactivation, previous studies have addressed functional reciprocal connectivity between primary auditory cortex (A1) and the anterior and posterior auditory fields (AAF and PAF), as well as second auditory cortex (A2; Carrasco and Lomber 2009a, 2010). However, functional interactions for higher order fields of...

Multisensory responses in a belt region of the dorsal auditory cortical pathway

“…Activity of DZ neurons is based on the interplay of intrinsic neuronal properties, local circuit processing and input signals. As expected from the dominant presence of auditory responsivity, inputs to DZ largely arise from auditory cortical and thalamic regions (Kok et al, 2015; Winer et al, 2001). However, a report by Kok et al (2013) identified projections from 18 visual cortical areas whose inputs represented >38% of the total cortical inputs to DZ.…”

What can we learn from inactivation studies? Lessons from auditory cortex

“…Most studies to date aimed to inactivate primary AC (A1) as it is most clearly stereotaxically- and cytoarchitectonically-defined and is the region with most well-defined homologues in other species [ 32 ]. The hierarchical organisation of auditory cortex means that disrupting primary cortex will additionally perturb processing in non‐primary areas [ 33 , 34 ]. Despite A1 being the most frequently targeted inactivation site, the trade-off between incomplete inactivation within an area and nonspecific effects beyond a target area make it likely that non‐primary auditory fields ( Figure 1 A) are usually at least partially affected as well, thus obfuscating the exact role of A1.…”

Reversible Cooling-induced Deactivations to Study Cortical Contributions to Obstacle Memory in the Walking Cat

“…With proper use and care, implanted cryoloops can be cooled routinely for many years. These cortical cooling procedures can be adapted to other behavioral paradigms 10,11,12 or electrophysiological recording preparations 13,14 in alternative animal models 15,17,18,22 .…”

“…. NOTE: This can be verified with thermocline mapping 12 or with a thermal imaging camera 13,14,19 .…”

“…Such deactivation can be reversed simply by ceasing the flow of methanol. This method has been used to study cortical contributions to sensory processing and behaviors 9,10,11,12,13,14,15,16,17 , as well as the motor control of saccadic eye movements 18 and memory-guided obstacle locomotion 19 .…”