Elsevier

Neuroscience

Volume 143, Issue 4, 28 December 2006, Pages 1065-1083
Neuroscience

Systems neuroscience
Multisensory processing via early cortical stages: Connections of the primary auditory cortical field with other sensory systems

https://doi.org/10.1016/j.neuroscience.2006.08.035Get rights and content

Abstract

It is still a popular view that primary sensory cortices are unimodal, but recent physiological studies have shown that under certain behavioral conditions primary sensory cortices can also be activated by multiple other modalities. Here, we investigate the anatomical substrate, which may underlie multisensory processes at the level of the primary auditory cortex (field AI), and which may, in turn, enable AI to influence other sensory systems. We approached this issue by means of the axonal transport of the sensitive bidirectional neuronal tracer fluorescein-labeled dextran which was injected into AI of Mongolian gerbils (Meriones unguiculatus).

Of the total number of retrogradely labeled cell bodies (i.e. cells of origin of direct projections to AI) found in non-auditory sensory and multisensory brain areas, approximately 40% were in cortical areas and 60% in subcortical structures. Of the cell bodies in the cortical areas about 82% were located in multisensory cortex, viz., the dorsoposterior and ventroposterior, posterior parietal cortex, the claustrum, and the endopiriform nucleus, 10% were located in the primary somatosensory cortex (hindlimb and trunk region), and 8% in secondary visual cortex. The cortical regions with retrogradely labeled cells also contained anterogradely labeled axons and their terminations, i.e. they are also target areas of direct projections from AI. In addition, the primary olfactory cortex was identified as a target area of projections from AI. The laminar pattern of corticocortical connections suggests that AI receives primarily cortical feedback-type inputs and projects in a feedforward manner to its target areas.

Of the labeled cell bodies in the subcortical structures, approximately 90% were located in multisensory thalamic, 4% in visual thalamic, and 6% in multisensory lower brainstem structures. At subcortical levels, we observed a similar correspondence of retrogradely labeled cells and anterogradely labeled axons and terminals in visual (posterior limitans thalamic nucleus) and multisensory thalamic nuclei (dorsal and medial division of the medial geniculate body, suprageniculate nucleus, posterior thalamic cell group, zona incerta), and in the multisensory nucleus of the brachium of the inferior colliculus. Retrograde, but not anterograde, labeling was found in the multisensory pontine reticular formation, particularly in the reticulotegmental nucleus of the pons. Conversely, anterograde, but no retrograde, labeling was found in the visual laterodorsal and lateroposterior thalamic nuclei, in the multisensory peripeduncular, posterior intralaminar, and reticular thalamic nuclei, as well as in the multisensory superior and pericentral inferior colliculi (including cuneiform and sagulum nucleus), pontine nuclei, and periaqueductal gray.

Our study supports the notion that AI is not merely involved in the analysis of auditory stimulus properties but also in processing of other sensory and multisensory information. Since AI is directly connected to other primary sensory cortices (viz. the somatosensory and olfactory ones) multisensory information is probably also processed in these cortices. This suggests more generally, that primary sensory cortices may not be unimodal.

Section snippets

Experimental procedures

Twelve young adult male Mongolian gerbils (Meriones unguiculatus), at least four months old and weighing 80–100 g, were used for this study. All experiments were approved by the animal care committee of Sachsen-Anhalt, Germany (No. 43.2-42502/2-2-325 IFN MD), in accordance with the NIH Guide for the Care and Use of Laboratory Animals (1996). Every attempt was made to minimize the number of animals used and to reduce their suffering at all stages of the study.

Results

The data presented here result from small injections of FD into the left AI. The injection sites were roughly spherical (mean diameter of 257±31 μm) and covered several cortical layers, usually supragranular, granular, and infragranular layers, but never reached layer VI or the white matter (Table 1). Four representative injection sites are illustrated in Fig. 1D. The approximate BFs of neurons at the injection sites ranged from 0.25 kHz to 12 kHz in the different cases (Table 1) and were

Summary and comparison with previous studies in the gerbil

The present study has shown, by use of the bidirectional and sensitive neuronal tracer FD, that AI of the gerbil (1) receives direct inputs from somatosensory, visual, and multisensory cortices, as well as from visual and multisensory thalamic and brainstem structures, and (2) has various projections to somatosensory, olfactory, visual, and multisensory cortical and subcortical brain regions. These connections are summarized in Fig. 4A. The results of the present study confirm some of the

Conclusions

In conclusion, it becomes increasingly apparent that the concept of purely unimodal processing in primary sensory cortices is wrong. Even these primary areas are not mere analyzers of properties of stimuli of their own modality but rather are involved in complex processing of other sensory, multisensory, and non-sensory information (for discussions see also Shimojo and Shams 2001, Cappe and Barone 2005, Scheich et al 2005, Schroeder and Foxe 2005).

Acknowledgments

We thank I. Forner, A. Gürke, and K. Gruss for their excellent histological assistance, Dr. W. Zuschratter for the technical support during the confocal laser scannings, M. Schild for reconstructing the ORIS data, and I. W. Stürmer for his investigation of the gerbil drumming behavior. We are also grateful to the three anonymous reviewers who provided helpful comments on a previous version of this paper.

Supported by the State Sachsen-Anhalt, BMBF, and DFG (SFB TR 31), Germany.

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