Research paperCortical and thalamic connectivity of the auditory anterior ectosylvian cortex of early-deaf cats: Implications for neural mechanisms of crossmodal plasticity
Introduction
Individuals who experience profound sensory loss early in life often exhibit dramatic functional neurological changes that lead to perceptual and behavioral improvements in the remaining senses. Regarded as ‘adaptive’ or ‘compensatory plasticity,’ these behavioral effects have been reported for early-blind or early-deaf humans for a variety of sensory tasks (for review, see Merabet and Pascual-Leone, 2010, Frasnelli et al., 2011). In a broader context, the phenomenon where the representation of a damaged or lost sensory modality is replaced by the remaining, intact modalities is termed ‘crossmodal plasticity’ and this functional effect has been confirmed in experimental animals. In a seminal series of experiments on compensatory plasticity, visually-deprived cats demonstrated auditory localization behaviors which exceeded that present in normally-sighted controls. Furthermore, a region of normally visual cortex not only showed auditory crossmodal plasticity in visually deprived animals, but also contained auditory neurons with supranormal localization sensitivities (e.g., Rauschecker and Korte, 1993, Korte and Rauschecker, 1993).
Compared to the volume of studies of vision loss, few experimental investigations of the crossmodal effects of early deafness have been conducted, until recently. Congenitally deaf mice have been shown to exhibit both visual and somatosensory responses in the primary auditory (A1) area, as well as an expanded representation of the primary visual area (Hunt et al., 2006). In early-deaf ferrets, auditory cortical fields including A1 and the anterior auditory field (AAF) exhibited somatosensory-evoked activity (Meredith and Allman, 2012). In congenitally deaf cats, visual crossmodal plasticity has been identified in the dorsal auditory zone (DZ) and the posterior auditory field (PAF; Lomber et al., 2010, Lomber et al., 2011), but not in A1 (Kral et al., 2003), while both visual and somatosensory crossmodal reorganization has been demonstrated in the AAF and the auditory field of the anterior ectosylvian sulcus (FAES) of early-deaf cats (Meredith and Lomber, 2011, Meredith et al., 2011).
To date, one of the most comprehensively studied auditory regions to demonstrate crossmodal plasticity is the FAES. In hearing cats, the FAES contains a mixture of auditory (∼77%) and non-auditory (∼33%; mostly in the form of auditory-visual, and auditory-somatosensory multisensory neurons; Meredith et al., 2011) and many FAES neurons are characterized by sensitivity to acoustic location (Clarey and Irvine, 1990a, Korte and Rauschecker, 1993, Xu et al., 1998, Las et al., 2008) and sound movement (Jiang et al., 2000). Connections from auditory cortical sources dominate inputs to the FAES, especially from areas AAF and DZ (Lee and Winer, 2008) while non-auditory afferents arrive largely from somatosensory area SIV (Meredith et al., 2006) and the visual lateral suprasylvian areas (Clarey and Irvine, 1990b). The FAES is the major source of auditory corticotectal projections (Meredith and Clemo, 1989, Chabot et al., 2013) and, therefore, plays an important role in mediating superior colliculus (SC) function and behaviors (Meredith and Clemo, 1989, Wallace et al., 1993, Malhotra et al., 2004, Meredith et al., 2011). Accordingly, reversible deactivation of the FAES in hearing cats blocks accurate orienting and localization behaviors to auditory stimuli (Malhotra et al., 2004, Meredith et al., 2011). In early-deaf cats, auditory-evoked activity in the FAES is replaced by visual (∼70% of neurons) and somatosensory (∼30%) responses (Meredith et al., 2011). Although a visuotopic organization was not observed, visual receptive fields displayed complex response properties such as direction and velocity preferences and, collectively, represented the central and contralateral visual field. Ultimately, the crossmodal visual representation in the early-deaf FAES is critical for visuomotor function, since reversible deactivation resulted in the loss of accurate orienting and localization behaviors to contralateral visual cues in early-deaf, but not hearing controls (Meredith et al., 2011). However, little is known about the connectional basis subserving deafness-induced crossmodal plasticity in the FAES.
The mechanisms underlying the phenomenon of crossmodal plasticity have long been the subject of discussion and speculation. In a review, Rauschecker (1995) summarized the logical possibilities that could provide a connectional substrate for the phenomenon: crossmodal plasticity could result from the recruitment of new projections from novel areas, by increased projections from existing sources, or by the ‘unmasking’ of existing crossmodal inputs. The present experiment sought to test these possibilities by making tracer injections into the crossmodally-reorganized FAES of early-deaf cats to identify the distribution and proportional strength of input sources to the region, and comparing these results to data obtained by similar tracer injections made into FAES of hearing animals.
Section snippets
Materials and methods
All procedures were performed in compliance with the Guide for Care and Use of Laboratory Animals (National Institutes of Health, publication 86-23), the National Research Council's Guidelines for Care and Use of Mammals in Neuroscience and Behavioral Research (2003) with prior approval by the Institutional Animal Care and Use Committee at Virginia Commonwealth University. Also, all procedures were conducted in accord with the Canadian Council on Animal Care's Guide to the Care and Use of
Injection sites
As noted in earlier studies of the anterior ectosylvian region (Clemo and Stein, 1983, Clemo and Stein, 1985, Meredith and Clemo, 1989), this sulcal cortex is highly variable from animal to animal, and sometimes may even fail to invaginate under the middle ectosylvian gyrus (which becomes apparent only after tissue processing). Another complication for examination of this region is that the FAES resides in close proximity to, and shares a common border with, the visual area of the ectosylvian
Discussion
Until very recently, the mechanisms underlying crossmodal plasticity have received more speculation than empirical examination. As proposed by Rauschecker (1995) and reiterated by numerous publications and reviews, when activation from a major sensory system is lost or damaged, crossmodal replacements might result from enhanced ingrowth of new projections, or from increased projections from existing sources, or from the ‘unmasking’ of existing inputs that were otherwise silent. The first two of
Conclusion
The observations presented by this work strongly indicate that crossmodal plasticity in the FAES, like other regions of deafened auditory cortex, is subserved by features of existing connections instead of generation projections from novel non-auditory sources. Furthermore, the projections to the FAES occur in essentially similar proportions in both hearing and early-deaf animals, which suggests that connections maintained between ‘auditory’ cortical regions after hearing loss are also likely
Conflicts of interest
The authors have no conflict of interest regarding this work.
Role of authors
All authors had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design (MAM). Acquisition of data: (MAM, NC, SMC). Analysis and interpretation of data: (MAM; SMC, HRC). Drafting of the manuscript: (MAM). Critical revision of the manuscript for important intellectual content: (MAM, HRC, SGL). Statistical analysis: (MAM). Obtained funding: (MAM, SGL). Administrative, technical, and material
Acknowledgments
This work was supported by the National Institutes of Health Grant (NS-39460; MAM) and the Virginia Commonwealth University Presidential Research Initiatives Program (MAM), the Canadian Institutes of Health Research (SGL), and the Natural Sciences and Engineering Research Council of Canada (SGL). We thank S. Ramoa and K. McKee for assistance with data collection, M. Kok for assistance in mapping cortical area functional distributions and M. Kok and C. Wong for reading the manuscript.
References (71)
- et al.
Cerebral origins of the auditory projection to the superior colliculus of the cat
Hear Res.
(2013) - et al.
Crossmodal plasticity in sensory loss
Prog. Brain Res.
(2011) - et al.
Multisensory plasticity in congenitally deaf mice: how are cortical areas functionally specified?
Neuroscience
(2006) - et al.
Responses of cells to stationary and moving sound stimuli in the anterior ectosylvian cortex of cats
Hear Res.
(2000) Auditory critical periods: a review from system's perspective
Neuroscience
(2013)- et al.
Vibration-induced auditory-cortex activation in a congenitally deaf adult
Curr. Biol.
(1998) - et al.
Adaptive crossmodal plasticity in deaf auditory cortex: areal and laminar contributions to supranormal vision in the deaf
Prog. Brain Res.
(2011) - et al.
Areas of cat auditory cortex as defined by neurofilament proteins expressing SMI-32
Hear Res.
(2010) - et al.
Somatosensory and visual crossmodal plasticity in the anterior auditory field of early-deaf cats
Hear Res.
(2011) Compensatory plasticity and sensory substitution in the cerebral cortex
Trends Neurosci.
(1995)
Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies
J. Neurosci. Methods
Profound hearing loss in the cat following the single co-administration of kanamycin and ethacrynic acid
Hear Res.
Adult deafness induces somatosensory conversion of ferret auditory cortex
Proc. Natl. Acad. Sci. (USA)
Vibrotactile activation of the auditory cortices in deaf versus hearing adults
Neuroreport
Organization of the association cortical afferent connections of area 5: a retrograde tracer study in the cat
J. Comp. Neurol.
Reorganization of the connectivity of cortical field DZ in congenitally deaf cat
PLoS One
Cross-modal plasticity: where and how?
Nat. Rev. Neurosci.
Visual and auditory association areas of the cat's posterior ectosylvian gyrus: thalamic afferents
J. Comp. Neurol.
Emergence and refinement of clustered horizontal connections in cat striate cortex
J. Neurosci.
The thalamocortical projection systems in primate: an anatomical support for multisensory and sensorimotor interplay
Cereb. Cortex
Dissociating cognitive and sensory neural plasticity in human superior temporal cortex
Nat. Comm.
Differential modification of cortical and thalamic projections to cat primary auditory cortex following early- and late-onset deafness
J. Comp. Neurol.
The anterior ectosylvian sulcal auditory field in the cat: I. An electrophysiological study of its relationship to surrounding auditory cortical fields
J. Comp. Neurol.
The anterior ectosylvian sulcal auditory field in the cat: II. A horseradish peroxidase study of its thalamic and cortical connections
J. Comp. Neurol.
Insular cortex and neighboring fields in the cat: a redefinition based on cortical microarchitecture and connections with the thalamus
J. Comp. Neurol.
Sensory and multisensory representations within the cat rostral suprasylvian cortices
J. Comp. Neurol.
Synaptic basis for crossmodal plasticity: enhanced supragranular dendritic spine density in anterior extosylvian auditory cortex of the early deaf cat
Cereb. Cortex
Cortico-cortical relations of cat somatosensory areas SIV and SV
Somatosens. Mot. Res.
Organization of a fourth somatosensory area of cortex in cat
J. Neurophysiol.
Effects of cooling somatosensory cortex on response properties of tactile cells in the superior colliculus
J. Neurophysiol.
Extrinsic visual and auditory cortical connections in the 4-day-old kitten
J. Comp. Neurol.
Functional selectivity in sensory deprived cortices
J. Neurophysiol.
Visual stimuli activate auditory cortex in the deaf
Nat. Neurosci.
Ultrastructural evidence for synaptic interactions between thalamocortical axons and subplate neurons
Eur. J. Neurosci.
GABAergic organization of the cat medial geniculate body
J. Comp. Neurol.
Cited by (38)
Connectome alterations following perinatal deafness in the cat
2024, NeuroImageCross-modal integration and plasticity in the superior temporal cortex
2022, Handbook of Clinical NeurologyInteraction of auditory and pain pathways: Effects of stimulus intensity, hearing loss and opioid signaling
2020, Hearing ResearchCitation Excerpt :In addition, it receives inputs from several auditory nuclei and responds to acoustic stimulation (Halladay and Blair, 2012; McNally et al., 2004; Parsons et al., 2014; Radmilovich et al., 1991; Wang et al., 2019). Cochlear hearing loss can give rise to neuroplastic changes in the central nervous system leading to profound changes in neural function in brain regions associated with sensory processing and multisensory integration (Allman et al., 2009; Bizley and King, 2009; Meredith and Allman, 2012, 2016; Moshourab et al., 2017; Shore et al., 2008; Zeng et al., 2012). To determine if noise-induced hearing loss might disrupt thermal pain sensitivity, we measured thermal TF latencies before and after inducing a significant unilateral hearing loss (Fig. 5).
Crossmodal reorganisation in deafness: Mechanisms for functional preservation and functional change
2020, Neuroscience and Biobehavioral Reviews
- 1
Present address: Department of Dermatology, University of North Carolina, Chapel Hill, NC 27516, USA.