Areal and laminar organization of corticocortical projections in the rat somatosensory cortex.

The present study examines patterns of connectivity between the primary somatosensory cortex of the rat (SI) and surrounding cortical areas also implicated in the processing of somatosensory information. The impetus for the study was the recent reports of major differences in the organization of cortex lateral and caudal to the SI in two other rodent species; the mouse (Carvell and Simons, '86: Somatosens. Res. 3:213-237; '87: J. Comp. Neurol. 265:409-427) and the grey squirrel (Krubitzer et al., '86: J. Comp. Neurol 250: 403-430). Corticocortical connections between the somatosensory areas of the rat parietal cortex were examined by using the combined retrograde and anterograde transport of horseradish peroxidase as well as the retrograde transport of fluorescent tracers. Tracer injections were made into different locations within SI and dysgranular cortex as well as into more lateral regions of parietal cortex. The tangential patterns of distribution both of callosal connections and of cytochrome oxidase activity together provided points of reference in determining the relation between injection sites and the resultant patterns of label. The results indicate that two distinct somatosensory areas, SI and the dysgranular cortex, are interconnected with a further lateral somatosensory area referred to as the second somatosensory area (SII). These projections are organized in a topographic fashion, which we interpret as evidence for a single representation of the body surface in SII. The three somatosensory areas each exhibit unique laminar patterns of ipsilateral corticocortical projection neurons and terminations. In SI, projection neurons are found mainly in layers II, III, and Va, and terminations are largely restricted to the infragranular layers. In the dysgranular cortex, projection neurons and terminations are found in all layers except layer I in which only terminal label is detectable and layer Vb in which notably fewer neurons are labelled. In SII, projection neurons and terminations are found in all layers except layer I and are particularly dense in lower layer III and layer IV. Further, whereas the laminar and areal distributions of ipsilateral and contralateral corticocortical projections largely overlap in both SI and the dysgranular cortex, in SII they tend to be areally segregated. Neurons projecting bilaterally to both ipsilateral and contralateral somatosensory cortex were equally rare in all three somatosensory areas. These results are discussed in relation to the organization of SII in other rodent species, and it is concluded that in the rat, like the mouse, cortex lateral and caudal to SI contains a single representation of the body surface.

Laminar and areal differences in the origin of the subcortical projection neurons of the rat somatosensory cortex.

Fluorescent retrograde tracing techniques were employed in a double-labelling paradigm to determine the distribution of corticospinal, corticotectal, and corticotrigeminal projection neurons in layer Vb of the adult and neonatal rat somatosensory cortex. The double-labelling paradigm allowed a direct comparison of the cortical distribution of neurons projecting to each target and identification of neurons projecting to more than one target. In the adult rat, each population of projection neurons was found to have a unique laminar and/or areal distribution. Corticospinal projection neurons were located throughout the width of layer Vb in the medial granular portion of somatosensory cortex, while corticotrigeminal projection neurons were distributed throughout the width of layer Vb in the more laterally located dysgranular portion of somatosensory cortex. Corticotectal projection neurons were located more superficially in layer Vb than either corticospinal or corticotrigeminal projection neurons and found scattered throughout both dysgranular and granular somatosensory cortex. Each combination of subcortical injections also resulted in double labelling a small percentage of uniquely distributed neurons. These distribution differences coupled with measurements of cell size allowed us to identify the parent population of the dual projection neurons. Subpopulations of corticotectal neurons also project to the brainstem trigeminal complex and to the spinal cord. Subpopulations of corticotrigeminal neurons also project to the spinal cord, and a proportion of corticotrigeminal neurons projects to at least two targets within the brainstem trigeminal complex (nucleus principalis and subnucleus interpolaris). In the adult rat, corticospinal neurons (as defined by either laminar position or somal size) did not appear to give off collaterals to either the superior colliculus or brainstem trigeminal complex. In the neonatal rat, double-labelled neurons which project to both the spinal cord and the tectum are distributed throughout the full width of layer Vb, rather than restricted to the superficial portion of the layer as in the adult rat. Further, it appears as if the ontogenetic change in the laminar distribution of corticospinal and tectal projection neurons is achieved by mechanisms of selective process elimination rather than cell death. These results are discussed in terms of both the developmental factor which may contribute to the discrete distribution of cortical projection neurons found in the adult and the functional significance of bifurcating projection neurons.

Evidence for two complementary patterns of thalamic input to the rat somatosensory cortex.

We provide evidence that the thalamic projections originating from the medial portion of the posterior thalamic complex to the somatosensory cortex of the rat are distributed in a detailed pattern which is complementary to the pattern of projections which originate in the ventral posterior nucleus.

Callosal projections in rat somatosensory cortex are altered by early removal of afferent input.

During the first postnatal week, the distribution of callosal projection neurons in the rat somatosensory cortex changes from a uniform to a discontinuous pattern. To determine if this change is influenced by afferent inputs to the somatosensory cortex, the effect of both early unilateral infraorbital nerve section and unilateral removal of the dorsal thalamus on the distribution of callosal projections in rat somatosensory cortex was examined. One month after either of the above manipulations at birth, the tangential distribution of callosal projections in the somatosensory cortex was examined using the combined retrograde and anterograde transport of horseradish peroxidase. Both manipulations alter the distribution of callosal projection neurons and terminations in the somatosensory cortex. After infraorbital nerve section, the distribution of callosal projections is altered in the contralateral primary somatosensory cortex. The abnormalities observed are consistent with the altered distribution of thalamocortical projections. In addition, consistent abnormalities were observed in the pattern of callosal projections of the second somatosensory area of both hemispheres. Most notably, they are absent in a portion of the region that contains the representation of the mystacial vibrissae and sinus hairs in this area. Thalamic ablation resulted in highly aberrant patterns of callosal projections in the somatosensory cortex on the operated side, where abnormal bands and clusters of callosal projections were observed in apparently random locations. These results are interpreted as evidence that both peripheral and central inputs influence the maturational changes in the distribution of callosal projection neurons.