Reorganization of the Connectivity of Cortical Field DZ in Congenitally Deaf Cat

Abstract

Psychophysics and brain imaging studies in deaf patients have revealed a functional crossmodal reorganization that affects the remaining sensory modalities. Similarly, the congenital deaf cat (CDC) shows supra-normal visual skills that are supported by specific auditory fields (DZ-dorsal zone and P-posterior auditory cortex) but not the primary auditory cortex (A1). To assess the functional reorganization observed in deafness we analyzed the connectivity pattern of the auditory cortex by means of injections of anatomical tracers in DZ and A1 in both congenital deaf and normally hearing cats. A quantitative analysis of the distribution of the projecting neurons revealed the presence of non-auditory inputs to both A1 and DZ of the CDC which were not observed in the hearing cats. Firstly, some visual (areas 19/20) and somatosensory (SIV) areas were projecting toward DZ of the CDC but not in the control. Secondly, A1 of the deaf cat received a weak projection from the visual lateral posterior nuclei (LP). Most of these abnormal projections to A1 and DZ represent only a small fraction of the normal inputs to these areas. In addition, most of the afferents to DZ and A1 appeared normal in terms of areal specificity and strength of projection, with preserved but smeared nucleotopic gradient of A1 in CDCs. In conclusion, while the abnormal projections revealed in the CDC can participate in the crossmodal compensatory mechanisms, the observation of a limited reorganization of the connectivity pattern of the CDC implies that functional reorganization in congenital deafness is further supported also by normal cortico-cortical connectivity.

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

“…DZ receives projections from dorsal MGN (He and Hashikawa 1998;Lee and Winer 2008a;Barone et al 2013), which in turn receives input from the ascending auditory tract via the inferior colliculus (Winer 2011). Cortically, DZ receives input from AAF (Lee and Winer 2008b;Barone et al 2013;Kok et al 2014), which itself receives tonotopically organized input from ventral MGN (Winer et al 2001;Lee and Winer 2008a).…”

“…AAF receives weak input from PAF and although AAF receives strong input from A1 (Lee and Winer 2008b), previous studies have demonstrated that it is unsusceptible to A1 deactivation (Carrasco and Lomber 2009b). DZ similarly receives cortical input from auditory field of the anterior ectosylvian sulcus (fAES; Lee and Winer 2008b;Barone et al 2013;Kok et al 2014), which is the only dorsal auditory region lacking strong projections from A1, receives weak input from PAF (Lee and Winer 2008b) and also processes auditory spatial information (Malhotra et al 2004). A2 could be considered a candidate for possible sources contributing to the preservation of responses in DZ based on weak inputs from A1 and PAF with projections of moderate strength to DZ (Lee and Winer 2008b).…”

“…Furthermore, DZ has been suggested to form part of a functional auditory belt region because responses in DZ exhibit more complex frequency tuning and nonmonotonicity and have longer response latencies and broader tuning curves (Middlebrooks and Zook 1983;He et al 1997;Stecker et al 2005) than core regions A1 and AAF, which are characterized by simple, linear responses with short response latencies and sharp tuning curves (Sutter and Schreiner 1991;Stecker et al 2005;Carrasco and Lomber 2011). Thalamocortical connectivity analyses further support this designation (He and Hashikawa 1998), as thalamocortical projections to DZ in the cat (Lee and Winer 2008a) match those documented for belt regions of primate auditory cortex (Kaas et al 1999).Because A1 and PAF comprise two of the largest anatomical auditory cortical inputs to DZ (He and Hashikawa 1998;Lee and Winer 2008b;Barone et al 2013;Kok et al 2014) and because both cortical regions are known to be involved in auditory spatial processing (Fig. 1) (Stecker et al 2005;Malhotra and Lomber 2007;Malhotra et al 2008), we predicted that reversible deactivation of these areas would reduce neuronal response rates in DZ.…”

“…Because A1 and PAF comprise two of the largest anatomical auditory cortical inputs to DZ (He and Hashikawa 1998;Lee and Winer 2008b;Barone et al 2013;Kok et al 2014) and because both cortical regions are known to be involved in auditory spatial processing ( Fig. 1) (Stecker et al 2005;Malhotra and Lomber 2007;Malhotra et al 2008), we predicted that reversible deactivation of these areas would reduce neuronal response rates in DZ.…”

Distant heterotopic callosal connections to premotor cortex in non-human primates

“…One could deduce that this compensatory phenomenon of sensory substitution (see for example Rauschecker, 1995;Von Melchner et al, 2000;Finney et al, 2003;Lomber et al, 2010;Barone et al, 2013) points toward the role of the corpus callosum in cortical plasticity. However the speculative nature of these phenomena in humans warrants further experiments to become relevant in clinical practice.…”