Involvement of the caudal striatum in auditory processing: c-fos response to cortical application of picrotoxin and to auditory stimulation.

The topographical organization of corticostriatal connections have been postulated to follow a longitudinal pattern, each cortical area projecting on a longitudinal strip stretching along the whole rostro-caudal axis of the striatum. However, compared to the rostral striatal region, the caudal striatum exhibits distinct features in terms of connectivity and neuronal phenotype. The induction of c-fos expression in the striatum by cortical activation or sensory stimulation may throw more light on these functional corticostriatal relationships. In the present study, we examined the effects of cortical activation by local application of picrotoxin on the Fos-immunoreactivity (Fos-IR) in the striatum of the mouse, with special reference to the caudal part of the striatum. Activation of the auditory cortex induced a dense ipsilateral Fos-IR restricted to the caudal striatum i.e., in the caudo-medial striatum and in the caudal part of fundus striati, and a very sparse labelling in the medial region of the rostral striatum. Conversely, activation of both sensori-motor and visual cortices only resulted in Fos-IR in the main rostral part of the striatum, without response in the caudal extremity of the striatum. On the other hand, visual or auditory stimulation in awake animals failed to induce c-fos expression in the striatum. However, using quantitative in-situ hybridization for c-fos mRNA, we found that auditory, but not visual stimulation significantly potentiated the c-fos response to the D1 agonist SKF 38393 (2 mg/kg, i.p.) in the caudal part of the striatum. These functional observations suggest that, despite a more widespread cortico-striatal connection pattern deduced from tracing experiments, the strongest functional projections from the auditory system mainly converge onto a restricted part of the caudal striatum, according to a connection pattern that is reminiscent of the transverse segmentation proposed in early lesioning studies of corticostriatal projections.

[1]  Joseph E LeDoux,et al.  Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat , 1987, The Journal of comparative neurology.

[2]  Richard J Smeyne,et al.  Fos-IacZ transgenic mice: Mapping sites of gene induction in the central nervous system , 1992, Neuron.

[3]  S. Thorpe,et al.  Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus , 1983, Behavioural Brain Research.

[4]  D. Jacobowitz,et al.  Calcitonin gene-related peptide: Detailed immunohistochemical distribution in the central nervous system , 1985, Peptides.

[5]  T. Powell,et al.  The cortico-striate projection in the monkey. , 1970, Brain : a journal of neurology.

[6]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[7]  W. Nauta,et al.  Subcortical projections from the temporal neocortex in Macaca mulatta , 1956 .

[8]  E. Arnauld,et al.  Functional heterogeneity of the caudate-putamen as revealed by c-fos induction in response to D1 receptor activation. , 1993, Brain research. Molecular brain research.

[9]  F. Sharp,et al.  N-methyl-d-aspartate receptor activation in the neostriatum increases c-fos and fos-related antigens selectively in medium-sized neurons , 1991, Neuroscience.

[10]  H. Akil,et al.  Pattern and time course of immediate early gene expression in rat brain following acute stress , 1995, Neuroscience.

[11]  O Hikosaka,et al.  Functional properties of monkey caudate neurons. II. Visual and auditory responses. , 1989, Journal of neurophysiology.

[12]  J. McKenzie,et al.  Localization of binding sites for calcitonin gene-related peptide in rat brain by in vitro autoradiography , 1986, Neuroscience.

[13]  D. Bartel,et al.  Growth factors and membrane depolarization activate distinct programs of early response gene expression: dissociation of fos and jun induction. , 1989, Genes & development.

[14]  T. Curran,et al.  Mapping patterns of c-fos expression in the central nervous system after seizure. , 1987, Science.

[15]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  B. V. Updyke,et al.  Organization of visual corticostriatal projections in the cat, with observations on visual projections to claustrum and amygdala , 1993, The Journal of comparative neurology.

[17]  T. Kitama,et al.  Stimulation of the caudate nucleus induces contraversive saccadic eye movements as well as head turning in the cat , 1991, Neuroscience Research.

[18]  G. V. Van Hoesen,et al.  Widespread corticostriate projections from temporal cortex of the rhesus monkey , 1981, The Journal of comparative neurology.

[19]  M. Dragunow,et al.  D2 dopamine receptor antagonists induce fos and related proteins in rat striatal neurons , 1990, Neuroscience.

[20]  Joseph E. LeDoux,et al.  Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex , 1991, Neuroscience Letters.

[21]  Joseph E LeDoux,et al.  Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat , 1985, The Journal of comparative neurology.

[22]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[23]  A. Flaherty,et al.  Input-output organization of the sensorimotor striatum in the squirrel monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  T. Murphy,et al.  L-type voltage-sensitive calcium channels mediate synaptic activation of immediate early genes , 1991, Neuron.

[25]  W. Nauta,et al.  An intricately patterned prefronto‐caudate projection in the rhesus monkey , 1977, The Journal of comparative neurology.

[26]  Joseph E LeDoux,et al.  Topographic organization of neurons in the acoustic thalamus that project to the amygdala , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  M. West,et al.  Representation of the body by single neurons in the dorsolateral striatum of the awake, unrestrained rat , 1991, The Journal of comparative neurology.

[28]  M. Tohyama,et al.  Postnatal ontogeny of cells expressing prepro‐neurotensin/neuromedin N mRNA in the rat forebrain and midbrain: A hybridization histochemical study involving isotope‐labeled and enzyme‐labeled probes , 1991, The Journal of comparative neurology.

[29]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[30]  Joseph E LeDoux,et al.  Sensory tuning beyond the sensory system: an initial analysis of auditory response properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  J. Hedreen,et al.  Organization of striatopallidal, striatonigral, and nigrostriatal projections in the macaque , 1991, The Journal of comparative neurology.

[32]  D. Ginty,et al.  Induction of immediate early genes by Ca2+ influx requires cAMP-dependent protein kinase in PC12 cells. , 1991, The Journal of biological chemistry.

[33]  P. Emson,et al.  Topographic localization of calcitonin gene-related peptide in the rat brain: An immunohistochemical analysis , 1985, Neuroscience.

[34]  Y. Kubota,et al.  Striatal calcitonin gene-related peptide-like immunoreactive afferents from the regions ventral and medial to the medial geniculate nucleus of rats , 1991, Neuroscience.

[35]  M. Murer,et al.  Behavioral responses induced by electrical stimulation of the caudate nucleus in freely moving cats , 1993, Behavioural Brain Research.

[36]  E. Arnauld,et al.  Dopaminergic control of gene transcription during striatal ontogeny: c-fos induction by D1 receptor activation in the developing striosomes. , 1995, Brain research. Molecular brain research.

[37]  B. Ziółkowska,et al.  The NMDA receptor antagonist MK-801 markedly reduces the induction of c-fos gene by haloperidol in the mouse striatum , 1993, Neuroscience Letters.

[38]  C. Saper,et al.  Calcitonin gene‐related peptide (CGRP) immunoreactive projections from the thalamus to the striatum and amygdala in the rat , 1991, The Journal of comparative neurology.

[39]  T. Curran,et al.  Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. , 1991, Annual review of neuroscience.

[40]  P. Calabresi,et al.  Intrinsic membrane properties of neostriatal neurons can account for their low level of spontaneous activity , 1987, Neuroscience.

[41]  T. Hökfelt,et al.  Expression of c-Fos immunoreactivity in transmitter-characterized neurons after stress. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Lingzhi Fan,et al.  The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system , 1988, Neuroscience Letters.

[43]  T. Curran,et al.  Expression of c-fos protein in brain: metabolic mapping at the cellular level. , 1988, Science.

[44]  W. Nauta,et al.  The visual cortico-striato-nigral pathway in the rat , 1986, Neuroscience.

[45]  W. Nauta,et al.  The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods , 1982, Neuroscience.

[46]  I. Divac,et al.  Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibres in rat brain , 1981, Neuroscience.

[47]  T. Curran,et al.  Analysis of FBJ-MuSV provirus and c-fos (mouse) gene reveals that viral and cellular fos gene products have different carboxy termini , 1983, Cell.

[48]  C. W. Ragsdale,et al.  Fibers from the basolateral nucleus of the amygdala selectively innervate striosomes in the caudate nucleus of the cat , 1988, The Journal of comparative neurology.

[49]  A. Parent,et al.  Acetylcholinesterase-containing neurons in cat pallidal complex: morphological characteristics and projection towards the neocortex , 1981, Brain Research.

[50]  Joseph E. LeDoux,et al.  LTP is accompanied by commensurate enhancement of auditory-evoked responses in a fear conditioning circuit , 1995, Neuron.

[51]  Webster Ke Cortico-striate interrelations in the albino rat. , 1961 .

[52]  Michael Davis,et al.  Induction of the c-fos proto-oncogene in rat amygdala during unconditioned and conditioned fear , 1991, Brain Research.

[53]  R. M. Beckstead,et al.  Cortical stimulation induces Fos expression in striatal neurons , 1992, Neuroscience.

[54]  S. Hunt,et al.  Induction of c-fos-like protein in spinal cord neurons following sensory stimulation , 1987, Nature.

[55]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[56]  M. Roger,et al.  Anatomical study of the connections of the primary auditory area in the rat , 1989, The Journal of comparative neurology.

[57]  K. Johnson,et al.  Topographic patterns of brain activity in response to swim stress: assessment by 2-deoxyglucose uptake and expression of Fos-like immunoreactivity , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  R. Reale,et al.  Auditory cortical field projections to the basal ganglia of the cat , 1983, Neuroscience.

[59]  L. Aitkin,et al.  Auditory forebrain organization of an australian marsupial, the northern native cat (Dasyurus hallucatus) , 1989, The Journal of comparative neurology.

[60]  H. Nishijo,et al.  Rat amygdaloid neuron responses during auditory discrimination , 1993, Neuroscience.

[61]  T. Hattori,et al.  Separate neuronal populations of the rat globus pallidus projecting to the subthalamic nucleus, auditory cortex and pedunculopontine tegmental area , 1992, Neuroscience.

[62]  E. T. Rolls,et al.  Responses of striatal neurons in the behaving monkey. 2. Visual processing in the caudal neostriatum , 1984, Brain Research.

[63]  L. Brown Somatotopic organization in rat striatum: evidence for a combinational map. , 1992, Proceedings of the National Academy of Sciences of the United States of America.