0306-4522/7X/0901-0785102.00/O
Neurosci~ncr. Vol. 3. pp. 7X5-796. Pergamon PressLtd. 1978. Printedin GreatBritain. Q IBRO
SUBCORTICAL PROJECTIONS TO THE PREFRONTAL CORTEX IN THE RAT AS REVEALED BY THE HORSERADISH PEROXIDASE TECHNIQUE I.
DIVAC’
and ANNA K~MAL
Laboratory of Behavioral Physiology, Institute of Neurophysiology, Denmark
University of Copenhagen,
and A. BJ~~RKLUND and 0. LINDVALL Department of Histology, University of Lund, Sweden Abstract-The sources and distribution of subcortical afferents to the anterior neocortex were investigated in the rat using the horseradish peroxidase technique. Injections into the prefrontal cortex labelled, in addition to the mediodorsal thalamic nucleus, neurons in a total of fifteen subcortical nuclei, distributed in the basal telencephalon, claustrum, amygdala, thalamus, subthalamus, hypothalamus, mesencephalon and pons. Of these, the projections from the zona incerta, the lateroposterior thalamic nucleus, and the parabrachial region of the caudal mesencephalon to the prefrontal cortex have not previously been described. Different parts of the mediodorsal thalamic nucleus project to different areas of the frontal cortex. Thus, horseradish peroxidase injections in the most ventral pregenual part of the medial cortex labelled predominantly neurons in the medial anterior and dorsomedial posterior parts of the mediodorsal nucleus; injections into the more dorsal pregennal area labelled only neurons in the lateral and ventral parts of the nucleus; injections placed supragenually labelled neurons in the dorsolateral posterior part of the nucleus; and injections into the dorsal bank of the anterior rhinal sulcus labelled neurons in the centromedial part of the nucleus. Several other subcortical nuclei had projections overlapping with that of the mediodorsal thalamic nucleus. Five different types of such overlap were distinguished: (1) cell groups labelled after horseradish peroxidase injections into one of the subfields of the projection area of the mediodorsal nucleus (defined as the prefrontal cortex), but not outside this area (parataenial nucleus of the thalamus); (2) cell groups labelled both after injection into a subfield of the projection area of the mediodorsal nucleus and after injections in a restricted area outside this area (anteromedial, ventral and laterposterior thalamic nuclei); (3) cell groups labelled after injections into all subfields of the mediodorsal nucleus projection area, but not outside this area (ventral tegmental area, basolateral nucleus of amygdala); (4) cell groups labelled after injections into any area of the anterior neocortex, including the mediodorsal nucleus projection area (parabrachial neurons of the posterior mesencephalon); (5) cell groups labelled after all neocortical injections investigated (claustrum, magnocellular nuclei of the basal forebrain, lateral hypothalamus, zona incerta, intralaminar thalamic nuclei, nuclei raphe dorsalis and centralis superior, and locus coeruleus). We can draw the following conclusions from these and related findings. First, because of the apparent overlap of projections of the mediodorsal, the anteromedial and ventral thalamic nuclei in the rat, parts of the prefrontal cortex can also be called ‘cingulate’ and ‘premotor’. Second, on the basis of projections from parts of the mediodorsal nucleus, the prefrontal cortex of the rat can be subdivided into areas corresponding to those in other species. Third, the neocortex receives afferents from a large number of subcortical cell groups outside the thalamus, distributed from the telencephalon to thk pans; however, the prefrontal cortex seems to be the only neocortical area innervated by the ventral tegmental area and amygdala. Finally, neither the prefrontal cortex nor the mediodorsal thalamic nucleus receives afferents from regions directly involved in sensory and motor functions. CORTICAL
projections from principal thalamic nuclei have been suggested as an alternative to cytoarchitecture for subdivisions of the neocortex (MCCULLOCH,
’ Correspondence to: Ivan Divac, Institute of Neurophysiology, 36 Juliane Mariesvej, DK 2100 Copenhagen 0, Denmark ‘Trainee of European Training Program in Brain and Behaviour Research. Present address: Nencki Institute of Experimental Biology, Warsaw, Poland. Abbreviations: ABL, the basal amygdala nucleus; CL, claustrum; HL, lateral hypothalamus; HRP, horseradish
1944). According to this principle, the area which is innervated by the mediodorsal (MD) nucleus of the thalamus is the prefrontal cortex (ROSE & WOOJSEY, 1948; DIVAC, 1972). The validity of this approach to neocortical parcellation is supported by the fact that subdivision of the cortex on the basis of thalamic afferents has proved to be a better guide than cytoarchitecture in comparative studies of the functions of the prefrortal cortex (DIVAC, 1971; WIKMARK, DIVAC & WEISS, 1973). Since the relocation of the prefrontal cortex in the rat brain by LEONARD(1969), several anatomical studies have confirmed her initial findings
785
I. DIVAL. ANNA KOSMAL.A. BJBKI
Neurosci~ncr. Vol. 3. pp. 7X5-796. Pergamon PressLtd. 1978. Printedin GreatBritain. Q IBRO
SUBCORTICAL PROJECTIONS TO THE PREFRONTAL CORTEX IN THE RAT AS REVEALED BY THE HORSERADISH PEROXIDASE TECHNIQUE I.
DIVAC’
and ANNA K~MAL
Laboratory of Behavioral Physiology, Institute of Neurophysiology, Denmark
University of Copenhagen,
and A. BJ~~RKLUND and 0. LINDVALL Department of Histology, University of Lund, Sweden Abstract-The sources and distribution of subcortical afferents to the anterior neocortex were investigated in the rat using the horseradish peroxidase technique. Injections into the prefrontal cortex labelled, in addition to the mediodorsal thalamic nucleus, neurons in a total of fifteen subcortical nuclei, distributed in the basal telencephalon, claustrum, amygdala, thalamus, subthalamus, hypothalamus, mesencephalon and pons. Of these, the projections from the zona incerta, the lateroposterior thalamic nucleus, and the parabrachial region of the caudal mesencephalon to the prefrontal cortex have not previously been described. Different parts of the mediodorsal thalamic nucleus project to different areas of the frontal cortex. Thus, horseradish peroxidase injections in the most ventral pregenual part of the medial cortex labelled predominantly neurons in the medial anterior and dorsomedial posterior parts of the mediodorsal nucleus; injections into the more dorsal pregennal area labelled only neurons in the lateral and ventral parts of the nucleus; injections placed supragenually labelled neurons in the dorsolateral posterior part of the nucleus; and injections into the dorsal bank of the anterior rhinal sulcus labelled neurons in the centromedial part of the nucleus. Several other subcortical nuclei had projections overlapping with that of the mediodorsal thalamic nucleus. Five different types of such overlap were distinguished: (1) cell groups labelled after horseradish peroxidase injections into one of the subfields of the projection area of the mediodorsal nucleus (defined as the prefrontal cortex), but not outside this area (parataenial nucleus of the thalamus); (2) cell groups labelled both after injection into a subfield of the projection area of the mediodorsal nucleus and after injections in a restricted area outside this area (anteromedial, ventral and laterposterior thalamic nuclei); (3) cell groups labelled after injections into all subfields of the mediodorsal nucleus projection area, but not outside this area (ventral tegmental area, basolateral nucleus of amygdala); (4) cell groups labelled after injections into any area of the anterior neocortex, including the mediodorsal nucleus projection area (parabrachial neurons of the posterior mesencephalon); (5) cell groups labelled after all neocortical injections investigated (claustrum, magnocellular nuclei of the basal forebrain, lateral hypothalamus, zona incerta, intralaminar thalamic nuclei, nuclei raphe dorsalis and centralis superior, and locus coeruleus). We can draw the following conclusions from these and related findings. First, because of the apparent overlap of projections of the mediodorsal, the anteromedial and ventral thalamic nuclei in the rat, parts of the prefrontal cortex can also be called ‘cingulate’ and ‘premotor’. Second, on the basis of projections from parts of the mediodorsal nucleus, the prefrontal cortex of the rat can be subdivided into areas corresponding to those in other species. Third, the neocortex receives afferents from a large number of subcortical cell groups outside the thalamus, distributed from the telencephalon to thk pans; however, the prefrontal cortex seems to be the only neocortical area innervated by the ventral tegmental area and amygdala. Finally, neither the prefrontal cortex nor the mediodorsal thalamic nucleus receives afferents from regions directly involved in sensory and motor functions. CORTICAL
projections from principal thalamic nuclei have been suggested as an alternative to cytoarchitecture for subdivisions of the neocortex (MCCULLOCH,
’ Correspondence to: Ivan Divac, Institute of Neurophysiology, 36 Juliane Mariesvej, DK 2100 Copenhagen 0, Denmark ‘Trainee of European Training Program in Brain and Behaviour Research. Present address: Nencki Institute of Experimental Biology, Warsaw, Poland. Abbreviations: ABL, the basal amygdala nucleus; CL, claustrum; HL, lateral hypothalamus; HRP, horseradish
1944). According to this principle, the area which is innervated by the mediodorsal (MD) nucleus of the thalamus is the prefrontal cortex (ROSE & WOOJSEY, 1948; DIVAC, 1972). The validity of this approach to neocortical parcellation is supported by the fact that subdivision of the cortex on the basis of thalamic afferents has proved to be a better guide than cytoarchitecture in comparative studies of the functions of the prefrortal cortex (DIVAC, 1971; WIKMARK, DIVAC & WEISS, 1973). Since the relocation of the prefrontal cortex in the rat brain by LEONARD(1969), several anatomical studies have confirmed her initial findings
785
I. DIVAL. ANNA KOSMAL.A. BJBKI
