Non-sensory cortical and subcortical connections of the primary auditory cortex in Mongolian gerbils: bottom-up and top-down processing of neuronal information via field AI.
In the present study, we will provide further anatomical evidence that the primary auditory cortex (field AI) is not only involved in sensory processing of its own modality, but also in complex bottom-up and top-down processing of multimodal information. We have recently shown that AI in the Mongolian gerbil (Meriones unguiculatus) has substantial connections with non-auditory sensory and multisensory brain structures [Budinger, E., Heil, P., Hess, A., Scheich, H., 2006. Multisensory processing via early cortical stages: Connections of the primary auditory cortical field with other sensory systems. Neuroscience 143, 1065-1083]. Here we will report about the direct connections of AI with non-sensory cortical areas and subcortical structures. We approached this issue by means of the axonal transport of the sensitive bidirectional neuronal tracers fluorescein-labelled (FD) and tetramethylrhodamine-labelled dextran (TMRD), which were simultaneously injected into different frequency regions of the gerbil's AI. Of the total number of retrogradely labelled cell bodies found in non-sensory brain areas, which identify cells of origin of direct projections to AI, approximately 24% were in cortical areas and 76% in subcortical structures. Of the cell bodies in the cortical areas, about 4.4% were located in the orbital, 11.1% in the infralimbic medial prefrontal (areas DPC, IL), 18.2% in the cingulate (3.2% in CG1, 2.9% in CG2, 12.1% in CG3), 9.5% in the frontal association (area Fr2), 12.0% in the insular (areas AI, DI), 10.8% in the retrosplenial, and 34.0% in the perirhinal cortex. The cortical regions with retrogradely labelled cells, as well as the entorhinal cortex, also contained anterogradely labelled axons and their terminations, which means that they are also target areas of direct projections from AI. The laminar pattern of corticocortical connections indicates that AI receives primarily cortical feedback-type inputs and projects in a feedforward manner to its target areas. The high number of double-labelled somata, the non-topographic distribution of single FD- and TMRD-labelled somata, and the overlapping spatial distribution of FD- and TMRD-labelled axonal elements suggest rather non-tonotopic connections between AI and the multimodal cortices. Of the labelled cell bodies in the subcortical structures, about 38.8% were located in the ipsilateral basal forebrain (10.6% in the lateral amygdala LA, 11.5% in the globus pallidus GP, 3.7% in the ventral pallidum VPa, 13.0% in the nucleus basalis NB), 13.1% in the ipsi- and contralateral diencephalon (6.4% in the posterior paraventricular thalamic nuclei, 6.7% in the hypothalamic area), and 48.1% in the midbrain (20.0% in the ipsilateral substantia nigra, 9.8% in the ipsi- and contralateral ventral tegmental area, 5.0% in the ipsi- and contralateral locus coeruleus, 13.3% the ipsi- and contralateral dorsal raphe nuclei). Thus, the majority of subcortical inputs to AI was related to different neurotransmitter systems. Anterograde labelling was only found in some ipsilateral basal forebrain structures, namely, the LA, basolateral amygdala, GP, VPa, and NB. As for the cortex, the proportion and spatial distribution of single FD-, TMRD-, and double-labelled neuronal elements suggests rather non-tonotopic connections between AI and the neuromodulatory subcortical structures.
Budinger
Eike
E
Leibniz Institute for Neurobiology, Department of Auditory Learning and Speech, Brenneckestrasse 6, D-39118 Magdeburg, Germany. budinger@ifn-magdeburg.de
Laszcz
Anna
A
Lison
Holger
H
Scheich
Henning
H
Ohl
Frank W
FW
D000818:Animals; D001303:Auditory Cortex / Q000033:anatomy & histology*; D001370:Axonal Transport / Q000502:physiology; D001931:Brain Mapping; D003911:Dextrans / Q000378:metabolism; D019793:Fluorescein / Q000378:metabolism; D005849:Gerbillinae / Q000033:anatomy & histology*; D008297:Male; D009434:Neural Pathways / Q000033:anatomy & histology*; D009474:Neurons / Q000166:cytology / Q000378:metabolism
D003911:Dextrans; D019793:Fluorescein