R E S EA R C H A R T I C L E

Cortico-Cortical Connectivity Within Ferret Auditory Cortex Jennifer K. Bizley,1,2* Victoria M. Bajo,1 Fernando R. Nodal, and Andrew J. King1 1 2

Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, United Kingdom Ear Institute, University College London, London WC1X 8EE, United Kingdom

ABSTRACT Despite numerous studies of auditory cortical processing in the ferret (Mustela putorius), very little is known about the connections between the different regions of the auditory cortex that have been characterized cytoarchitectonically and physiologically. We examined the distribution of retrograde and anterograde labeling after injecting tracers into one or more regions of ferret auditory cortex. Injections of different tracers at frequency-matched locations in the core areas, the primary auditory cortex (A1) and anterior auditory field (AAF), of the same animal revealed the presence of reciprocal connections with overlapping projections to and from discrete regions within the posterior pseudosylvian and suprasylvian fields (PPF and PSF), suggesting that these connections are frequency specific. In

contrast, projections from the primary areas to the anterior dorsal field (ADF) on the anterior ectosylvian gyrus were scattered and non-overlapping, consistent with the non-tonotopic organization of this field. The relative strength of the projections originating in each of the primary fields differed, with A1 predominantly targeting the posterior bank fields PPF and PSF, which in turn project to the ventral posterior field, whereas AAF projects more heavily to the ADF, which then projects to the anteroventral field and the pseudosylvian sulcal cortex. These findings suggest that parallel anterior and posterior processing networks may exist, although the connections between different areas often overlap and interactions were present at all levels. J. Comp. Neurol. 523:2187–2210, 2015. C 2015 Wiley Periodicals, Inc. V

INDEXING TERMS: tract tracing; topography; auditory system; carnivore; multisensory

The ferret is now one of the most widely used animal models for studying auditory cortical processing and plasticity (reviewed by Nodal and King, 2014). 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). In contrast to the growing number of investigations into the physiological properties of cortical fields that C 2015 The Authors The Journal of Comparative Neurology Published by V

Wiley Periodicals, Inc.

lie beyond the auditory core, little attention has been paid to the anatomical organization of the nonprimary cortex in ferrets. By placing tracer deposits in the middle ectosylvian gyrus (MEG), previous studies have demonstrated the topography of the inputs from the medial geniculate nucleus (Pallas et al., 1990), and the presence of connections within and between this region and both the anterior and posterior parts of the gyrus (AEG

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. The copyright line for this article was changed on 18 August 2015 after original online publication. Grant sponsor: Wellcome Trust studentship (to J.K.B.); Grant sponsor: Sir Henry Dale Fellowship; Grant number: WT098418MA (to J.K.B.); Grant sponsor: Wellcome Trust Principal Research Fellowship; Grant number: WT076508AIA (to A.J.K.). *CORRESPONDENCE TO: J.K. Bizley, Ear Institute, University College London, 332 Grays Inn Road, London, WC1X 8EE, UK. E-mail: [email protected] Received November 6, 2014; Revised March 29, 2015; Accepted April 1, 2015. DOI 10.1002/cne.23784 Published online June 3, 2015 in Wiley (wileyonlinelibrary.com)

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TABLE 1. Injection Sites1 Animal no. 2

F0532

F0522 F0536 F0252 2

F0268

F0404 F0535 2

F0523

2

F0533

2

F0717 F0510 2 F0504 2 F0505

Tracer

IS location

FR BDA FR BDA FR FR BDA BDA FR CTB BDA CTB FR BDA FR BDA BDA CTB BDA CTB BDA BDA CTB

A1 AAF large A1/AAF A1/PSF A1 A1/AAF A1 AAF A1 A1/AAF AAF A1 AVF ADF AVF ADF VP PPF PSF AVF PPF AEG/aPSSC PPF

CF (kHz) 20 20 2 19 15 1 7 7 7 7 7 Noise 10 LED, noise

Cortico-Cortical Connectivity Within Ferret Auditory Cortex.

Despite numerous studies of auditory cortical processing in the ferret (Mustela putorius), very little is known about the connections between the diff...
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