Abstract
Intrinsic circuitry within the primary somatosensory cortex of the rat was examined in a combined light and electron microscope study. Corticothalamic projection neurons were retrogradely labeled by applying Phaseolus vulgaris leucoagglutinin (PHA-L) into the ventro-posteromedial thalamic nucleus (VPM). Most labeled neurons were pyramidal cells of layer VI. Postsynaptic targets of recurrent axon collaterals originating from these neurons were assessed in layers IV and V. Single labeled cells, complete with recurrent collaterals, could be isolated in “barrels” in which no anterograde transport had taken place. These findings were confirmed by first eliminating thalamocortical projections from the VPM with kainic acid and then applying PHA-L into the same nucleus. This procedure led to selective retrograde accumulation of tracer in layer VI pyramidal cells. Reconstructed portions of labeled axonal trees reached layer IV, bringing numerous boutons to layers IV, V and VI. The boutons had characteristic drumstick-like shapes. In order to identify postsynaptic targets, 4 sections of axons stemming from 3 neurons were reembedded and serially sectioned for electron microscopy. The ultrastructure of 72 asymmetric synapses, all belonging to identified collaterals, was analysed. Of the 72 terminals, 44 (59.5%) ended on dendritic spines and 30 on shafts of dendrites (40.5%). Perikarya were not among the targets. In a subset of the sample, the nature of the target neurons was examined by postembedding immunohistochemistry for γ-amino butyric acid (GABA) after staining for PHA-L. A total of 42 labeled terminals was found in layers IV and V; 23 (55%) were located on GABA-negative spines and 19 (45%) on dendritic shafts. Only 6 (32%) of the shafts were GABA-positive. The remaining ones were either clearly GABA-negative, or labeled only at background levels (n=13; 68%). The results show that most synapses of corticothalamic projection neurons found in layers IV and V terminate on spines and shafts of GABA-negative dendrites. This finding suggests that such recurrent collaterals are involved in both excitatory and inhibitory feedback mechanisms.
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References
Ahlsén G, Lindström S, Lo F-S (1985) Interaction beteween inhibitory pathways to principal cells in the lateral geniculate nuelceus of the cat. Exp Brain Res 58:134–143
Ahmed B, Anderson JC, Douglas RJ, Martin KAC, Nelson JC (1994) Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J Comp Neurol 341:39–49
Allison JD, Casagrande VA, Bonds AB (1995) The influence of input from the lower cortical layers on the orientation tuning of upper layer V1 cells in a primate. Vis Neurosci 12:309–320
Armstrong-James M, Welker E, Callahan CA (1993) The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat SI barrel cortex. J Neurosci 13:2149–2160
Bolz J, Gilbert CD (1986) Generation of end-inhibition in the visual cortex via interlaminar connections. Nature 320:362–365
Bolz J, Gilbert CD, Wiesel TN (1989) Pharmacological analysis of cortical circuitry. Trends Neurosci 12:292–296
Chmielowska J, Carvell GE, Simons DJ (1989) Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex. J Comp Neurol 285:325–338
Elhanany E, White EL (1990) Intrinsic circuitry: synapses involving the local axon collaterals of corticocortical projection neurons in the mouse primary somatosensory cortex. J Comp Neurol 291:43–54
Ferster D, Lindström S (1985) Augmenting responses evoked in area 17 of the cat by intracortical axon collaterals of corticogeniculate cells. J Physiol 367:217–232
Gilbert CD, Wiesel TN (1979) Morphology and intracortical projections of functionally characterized neurons in the cat visual cortex. Nature 280:120–125
Grieve KL, Sillito AM (1991a) The length summation properties of layer VI cells in the visual cortex and hypercomplex cell end zone inhibition. Exp Brain Res 84:319–325
Grieve KL, Sillito AM (1991b) A re-appraisal of the role of layer VI of the visual cortex in the generation of cortical end inhibition. Exp Brain Res 87:521–529
Grieve KL, Sillito AM (1995a) Non-length-tuned cells in layers II/III and IV of the visual cortex: the effect of blockade of layer VI on responses to stimuli of different lengths. Exp Brain Res 104:12–20
Grieve KL, Sillito AM (1995b) Differential properties of cells in the feline primary visual cortex providing the corticofugal feedback to the lateral geniculate nucleus and visual claustrum. J Neurosci 15:4868–4874
Hajós F, Staiger JF, Zilles K (1995) Geniculo-cortical synapses on vasoactive-intestinal-polypeptide (VIP) cells: a combined immunocytochemical and tracing study. Eur J Neurosci [Suppl] 8:16–31
Hirsch JA (1995) Synaptic integration in layer IV of the ferret striate cortex. J Physiol 483:183–199
Hodgson AJ, Penke B, Erdei A, Chubb IW, Somogyi P (1985) Antisera to gamma-aminobutyric acid. I. Production and characterization using a new model system. J Histochem Cytochem 33:229–239
Hoogland PV, Welker E, Loos H van der (1987) Organization of the projections from barrel cortex to thalamus in mice studied with Phaseolus vulgaris-leucoagglutinin and HRP. Exp Brain Res 68:73–87
Hubel DH, Wiesel TN (1962) Receptive field, binocular interaction and functional architecture in the cat's visual cortex. J Physiol 160:106–154
Kharazia VN, Weinberg RJ (1994) Glutamate in thalamic fibers terminating in layer IV of primary sensory cortex. J Neurosci 14:6021–6032
Kisvarday ZF, Martin KAC, Freund TF, Magloczky Zs, Whitteridge D, Somogyi P (1986) Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex. Exp Brain Res 64:541–552
Land PW, Buffer SA Jr, Yaskosky JD (1995) barreloids in adult rat thalamus: three-dimensional architecture and relationship to somatosensory cortical barrels. J Comp Neurol 355:573–588
McGuire BA, Hornung J-P, Gilbert CD, Wiesel TN (1984) Patterns of synaptic input to layer 4 of cat striate cortex. J Neurosci 4:3021–3033
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, Sydney
Sillito AM, Jones HE, Gerstein GL, West DC (1994) Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature 369:479–482
Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41:798–820
Somogyi P (1989) Synaptic organization of GABAergic neurons and GABA(A) receptors in the lateral geniculate nucleus and visual cortex. In: Lam DK-T, Gilbert CD (eds) Neural mechanisms of visual perception. Portfolio, Texas, pp 35–62
Somogyi P, Hodgson AJ (1985) Antisera to gamma-aminobutyric aicd. III. Demonstration of GABA in Golgi-impregnated neurons and conventional electron microscopic sections of cat striate cortex. J Histochem Cytochem 33:249–257
Staiger JF, Zilles K, Freund TF (1996) The innervation of VIP-immunoreactive neurons by the ventroposteromedial thalamic nucleus in the barrel cortex of the rat. J Comp Neurol 367:194–204
Waite PME, Tracey DJ (1995) Trigeminal sensory system. In: Paxinos G (ed) The rat nervous system. Academic Press, San Diego, pp 705–724
White EL, Czeiger D (1991) Synapses made by axons of callosal projection neurons in mouse somatosensory cortex: emphasis on intrinsic connections. J Comp Neurol 303:233–244
White EL, Keller A (1987) Intrinsic circuitry involving the local axon collaterals of corticothalamic projection cells in mouse SmI cortex. J Comp Neurol 262:13–26
Yuan B, Morrow TJ, Casey KL (1986) Corticofugal influences of SI cortex on ventrobasal thalamic neurons in the awake rat. J Neurosci 6:3611–3617
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Staiger, J.F., Zilles, K. & Freund, T.F. Recurrent axon collaterals of corticothalamic projection neurons in rat primary somatosensory cortex contribute to excitatory and inhibitory feedback-loops. Anat Embryol 194, 533–543 (1996). https://doi.org/10.1007/BF00187467
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DOI: https://doi.org/10.1007/BF00187467