Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study

The efferent projections of the infralimbic region (IL) of the medial prefrontal cortex of the rat were examined by using the anterograde transport of Phaseolus vulgaris leucoagglutinin (PHA-L). Major targets of the IL were found to include the agranular insular cortex, olfactory tubercle, perirhinal cortex, the whole amygdaloid complex, caudate putamen, accumbens nucleus, bed nucleus of the stria terminalis, midline thalamic nuclei, the lateral preoptic nucleus, paraventricular nucleus, supramammillary nucleus, medial mammillary nucleus, dorsal and posterior areas of the hypothalamus, ventral tegmental area, central gray, interpeduncular nucleus, dorsal raphe, lateral parabrachial nucleus and locus coeruleus. Previously unreported projections of the IL to the anterior olfactory nucleus, piriform cortex, anterior hypothalamic area and lateroanterior hypothalamic nucleus were observed. The density of labeled terminals was especially high in the agranular insular cortex, olfactory tubercle, medial division of the mediodorsal nucleus of the thalamus, dorsal hypothalamic area and the lateral division of the central amygdaloid nucleus. Several physiological and pharmacological studies have suggested that the IL functions as the 'visceral motor' cortex, involved in autonomic integration with behavioral and emotional events. The present investigation is the first comprehensive study of the IL efferent projections to support this concept.

[1]  J. A. Ricardo,et al.  Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat , 1978, Brain Research.

[2]  R. Norgren Projections from the nucleus of the solitary tract in the rat , 1978, Neuroscience.

[3]  A. Verberne,et al.  Medial prefrontal cortical lesions modulate baroreflex sensitivity in the rat , 1987, Brain Research.

[4]  Clifford B. Saper,et al.  Reciprocal parabrachial-cortical connections in the rat , 1982, Brain Research.

[5]  G. Leichnetz,et al.  Frontal cortical projections to the periaqueductal gray in the rat: A retrograde and orthograde horseradish peroxidase study , 1981, Neuroscience Letters.

[6]  J. Glowinski,et al.  Selective activation of the mesocortical DA system by stress , 1976, Nature.

[7]  H. Kita,et al.  Reciprocal connections between the lateral hypothalamus and the frontal cortex in the rat: Electrophysiological and anatomical observations , 1981, Brain Research.

[8]  D. Reis,et al.  The role of the solitary and paramedian reticular nuclei in mediating cardiovascular reflex responses from carotid baro‐ and chemoreceptors , 1972, The Journal of physiology.

[9]  R. T. Watson,et al.  Efferent Connections of the Rostral Portion of Medial Agranular Cortex in Rats , 1987, Brain Research Bulletin.

[10]  Bryan Kolb,et al.  Functions of the frontal cortex of the rat: A comparative review , 1984, Brain Research Reviews.

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

[12]  C. Saper,et al.  Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat , 1990, The Journal of comparative neurology.

[13]  E. Abercrombie,et al.  Differential Effect of Stress on In Vivo Dopamine Release in Striatum, Nucleus Accumbens, and Medial Frontal Cortex , 1989, Journal of neurochemistry.

[14]  R. Sullivan,et al.  The anterior midline cortex and adaptation to stress ulcers in rats , 1986, Brain Research Bulletin.

[15]  Sheng Chen,et al.  Afferent connections of the thalamic paraventricular and parataenial nuclei in the rat — a retrograde tracing study with iontophoretic application of Fluoro-Gold , 1990, Brain Research.

[16]  M. Cassell,et al.  Topography of projections from the medial prefrontal cortex to the amygdala in the rat , 1986, Brain Research Bulletin.

[17]  D. Reis,et al.  A role of insular cortex in cardiovascular function , 1987, The Journal of comparative neurology.

[18]  M. Herkenham The connections of the nucleus reuniens thalami: Evidence for a direct thalamo‐hippocampal pathway in the rat , 1978, The Journal of comparative neurology.

[19]  D. German,et al.  Medial prefrontal cortical projections to the region of the dorsal periventricular catecholamine system , 1981, Neuroscience.

[20]  M. Sarter,et al.  Convergence of basolateral amygdaloid and mediodorsal thalamic projections in different areas of the frontal cortex in the rat , 1983, Brain Research Bulletin.

[21]  T. van Groen,et al.  Extrinsic projections from area CA1 of the rat hippocampus: Olfactory, cortical, subcortical, and bilateral hippocampal formation projections , 1990, The Journal of comparative neurology.

[22]  C. Saper,et al.  Organization of cortical, basal forebrain, and hypothalamic afferents to the parabrachial nucleus in the rat , 1990, The Journal of comparative neurology.

[23]  R. Reep Relationship between prefrontal and limbic cortex: a comparative anatomical review. , 1984, Brain, behavior and evolution.

[24]  H. Fibiger,et al.  Cholinergic neurons of the laterodorsal tegmental nucleus: Efferent and afferent connections , 1986, The Journal of comparative neurology.

[25]  H. Groenewegen Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography , 1988, Neuroscience.

[26]  G. Aghajanian,et al.  Afferent projections to the rat locus coeruleus as determined by a retrograde tracing technique , 1978, The Journal of comparative neurology.

[27]  V. B. Domesick Projections from the cingulate cortex in the rat. , 1969, Brain research.

[28]  Clifford B. Saper,et al.  Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat , 1984, Brain Research Reviews.

[29]  T. Gray Autonomic Neuropeptide Connections of the Amygdala , 1989 .

[30]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[31]  H. Markowitsch,et al.  Cortical and thalamic afferent connections of the insular and adjacent cortex of the cat , 1983, The Journal of comparative neurology.

[32]  F E Bloom,et al.  The organization of projections from the cortes, amygdala, and hypothalamus to the nucleus of the solitary tract in rat , 1984, The Journal of comparative neurology.

[33]  A. Torvik,et al.  Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures. An experimental study in the rat , 1956, The Journal of comparative neurology.

[34]  C. Leonard,et al.  The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. , 1969, Brain research.

[35]  L. Hersh,et al.  Prefrontal cortical projections to the cholinergic neurons in the basal forebrain , 1991, The Journal of comparative neurology.

[36]  D. Hopkins,et al.  Mamillary body in the rat: Topography and synaptology of projections from the subicular complex, prefrontal cortex, and midbrain tegmentum , 1989, The Journal of comparative neurology.

[37]  H. Groenewegen,et al.  Phaseolus vulgaris leuco-agglutinin immunohistochemistry. A comparison between autoradiographic and lectin tracing of neuronal efferents , 1984, Brain Research.

[38]  R. M. Beckstead An autoradiographic examination of corticocortical and subcortical projections of the mediodorsal‐projection (prefrontal) cortex in the rat , 1979, The Journal of comparative neurology.

[39]  D. Cechetto,et al.  Autonomic responses and efferent pathways from the insular cortex in the rat , 1991, The Journal of comparative neurology.

[40]  Karl J. Zilles,et al.  The Cortex of the Rat: A Stereotaxic Atlas , 1985 .

[41]  G. Aghajanian,et al.  Habenular and other midbrain raphe afferents demonstrated by a modified retrograde tracing technique , 1977, Brain Research.

[42]  M. A. Siegel,et al.  Collateralization of the amygdaloid projections of the rat prelimbic and infralimbic cortices , 1989, The Journal of comparative neurology.

[43]  Rose Ce Functions of the prefrontal cortex. Behavioral investigations using ablation and electrophysiological techniques in rats, cats, dogs, and monkeys. , 1983 .

[44]  R. Passingham,et al.  Converging projections from the mediodorsal thalamic nucleus and mesencephalic dopaminergic neurons to the neocortex in three species , 1978, The Journal of comparative neurology.

[45]  M. Sarter,et al.  Collateral innervation of the medial and lateral prefrontal cortex by amygdaloid, thalamic, and brain‐stem neurons , 1984, The Journal of comparative neurology.

[46]  J. E. Rose,et al.  Structure and relations of limbic cortex and anterior thalamic nuclei in rabbit and cat , 1948, The Journal of comparative neurology.

[47]  M. Seki,et al.  Anterior thalamic afferents from the mamillary body and the limbic cortex in the rat , 1984, The Journal of comparative neurology.

[48]  K. Sripanidkulchai,et al.  The topography of the mesencephalic and pontine projections from the cingulate cortex of the rat , 1984, Brain Research.

[49]  D. Reis,et al.  Afferent projections to cardiovascular portions of the nucleus of the tractus solitarius in the rat , 1981, Brain Research.

[50]  B. Kolb,et al.  The Cerebral cortex of the rat , 1990 .

[51]  C. Saper Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus , 1984, The Journal of comparative neurology.

[52]  Y. Hosoya,et al.  Cells of origin of the descending afferents to the lateral hypothalamic area in the rat, studied with the horseradish peroxidase method , 1980, Neuroscience Letters.

[53]  J. Price,et al.  Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat , 1977, The Journal of comparative neurology.

[54]  J. Price,et al.  The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat , 1977, The Journal of comparative neurology.

[55]  G. Mogenson,et al.  Cardiovascular responses to electrical stimulation of the amygdala in the rat. , 1973, Experimental neurology.

[56]  J. Wyss,et al.  The involvement of the anterior cingulate cortex in blood pressure control , 1985, Brain Research.

[57]  C. Saper,et al.  Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat , 1987, The Journal of comparative neurology.

[58]  O. Ottersen,et al.  Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase , 1982, The Journal of comparative neurology.

[59]  L. Swanson,et al.  A direct projection from Ammon's horn to prefrontal cortex in the rat , 1981, Brain Research.

[60]  E. Neafsey,et al.  The medial frontal cortex and gastric motility: Microstimulation results and their possible significance for the overall pattern of organization of rat frontal and parietal cortex , 1986, Brain Research.

[61]  E. Grove,et al.  Neural associations of the substantia innominata in the rat: Afferent connections , 1988, The Journal of comparative neurology.

[62]  A. Siegel,et al.  The origin of the afferent supply to the mediodorsal thalamic nucleus: Enhancement of HRP transport by selective lesions , 1977, Brain Research.

[63]  E. Neafsey,et al.  The topographical organization of neurons in the rat medial frontal, insular and olfactory cortex projecting to the solitary nucleus, olfactory bulb, periaqueductal gray and superior colliculus , 1986, Brain Research.

[64]  M. Sarter,et al.  Convergence of intra‐ and interhemispheric cortical afferents: Lack of collateralization and evidence for a subrhinal cell group projecting heterotopically , 1985, The Journal of comparative neurology.

[65]  C. Saper,et al.  Convergence of autonomic and limbic connections in the insular cortex of the rat , 1982, The Journal of comparative neurology.

[66]  F. Wouterlood,et al.  Projection from the prefrontal cortex to histaminergic cell groups in the posterior hypothalamic region of the rat. Anterograde tracing withPhaseolus vulgaris leucoagglutinin combined with immunocytochemistry of histidine decar☐ylase , 1987, Brain Research.