The Organization and Connections of Second Somatosensory Cortex in the Agouti

Abstract

In order to understand how the mammalian sensory cortex has been structured during evolution, it is necessary to compare data from different species across distinct mammalian lineages. Here, we investigated the organization of the secondary somatosensory area (S2) in the agouti (Dasyprocta aguti), a medium-sized Amazonian rodent, using microelectrode mapping techniques and neurotracer injections. The topographic map obtained from multiunit electrophysiological recordings were correlated with both cytochrome oxidase (CO) histochemistry and with patterns of corticocortical connections in tangential sections. The electrophysiological mapping of the lateral strip of parietal cortex adjacent to the primary somatosensory area (S1) revealed that S2 displays a mirror-reversed topographical representation of S1, but with a smaller cortical magnification factor. The caudal border of S2 is surrounded by sensory fields which also respond to auditory stimulation. BDA injections into the forelimb representation of S2 revealed a dense homotopic ipsilateral projection to S1, supplemented by a less dense projection to the caudolateral cortex located near the rhinal sulcus (parietal rhinal area) and to a frontal region probably associated with the motor cortex. Our findings were similar to those described in other mammalian species, reinforcing the existence of a common plan of organization for S2 in the mammalian parietal cortex.

Keywords: S2; agouti; cortical connections; rodent; somatotopic map.

FIGURE 1

Agouti in its typical feeding posture, sitting on its hindlimbs (A). Dorsolateral view of the agouti’s brain with its lisencephalic aspect (B). Scale bar: 1 cm.

FIGURE 2

Topographic organization of primary (S1) and secondary (S2) somatosensory areas of the agouti. (A) Section of the flattened cortex, processed for cytochrome oxidase (CO) histochemistry, revealing the location of primary somatosensory (S1), auditory (A1), and visual (V1) areas, as well as the secondary somatosensory cortex (S2). (B) Micrograph amplification showing S1 and S2 (medial portion) (dotted rectangle in A). Electrolytic lesions are indicated by black arrows. The limit between S1 and S2 is defined as a narrow strip of less reactive tissue (white arrow). (C) Topographic map of S1 and S2 reconstructed from recording sites. The limits of distinct body representations are delimited by dashed lines. Continuous lines indicate the reversal of receptive field sequences across S1 and S2 (penetrations 1–13 and 14–27). (D) Drawing of the agouti’s body indicating the location of receptive fields illustrated in panel C. Grayscale codes indicate the difference in the size of receptive fields in both areas. Scale bars: A: 5 mm; B,C: 2 mm. Hl, hindlimb; Fl, forelimb; V, vibrissae; Ll, lower lip; Ul, upper lip; Tk, trunk; asterisk, electrolytic lesion; X, no response; LS, lateral sulcus.

FIGURE 3

Electrophysiological maps showing the organization of S2 and its relative location in the parietal cortex (inserts). S2 lies in a more lateral and posterior location in the parietal cortex, adjacent to the S1’s face representation, containing a complete representation of the contralateral sensory periphery, which is smaller and has a mirror-symmetrical orientation compared to S1 (A,B). Receptive fields for associated electrode penetrations in cases S2-03 and S2-04 (continuous lines in maps in A,B). The shaded areas in the schematic drawings indicate the receptive fields for corresponding electrode penetrations in the electrophysiological maps. Scale bars: 1 mm. Fl, forelimb; Hl, hindlimb; Ll, lower lip; N, nose; Tk, trunk; Ul, upper lip; V, vibrissae; X, no response.

FIGURE 4

Electrophysiological map (case S2-06) showing the location and organization of S2. Some bimodal responses were identified in a lateral region of S2, across the border with the auditory cortex. In more medial regions, beyond S1, it was possible to identify some visual responses. Notice the reversion in the progression of receptive field locations from S1 to S2 (continuous line) (A). The shaded areas in the schematic drawing indicate the receptive fields associated with corresponding electrode penetrations in the electrophysiological map, indicated by a continuous line (B). Scale bar: 1 mm. Fl, forelimb; Hl, hindlimb; Ll, lower lip; N, nose; Tk, trunk; Ul, upper lip; V, vibrissae; X, no response.

FIGURE 5

The cortical area occupied by the representation of different body parts in S2. (A) About half of S2 is devoted to the representation of the head, followed by the representation of limbs (forelimb: 23%; hindlimb: 17%) and trunk (10%). (B) Vibrissae (33%) and lower lip (32%) represent two thirds of the head’s representation, followed by the nose (24%) and upper lip (11%) (mean ± SEM).

FIGURE 6

Pattern of cytochrome oxidase (CO) reactivity across S1 area. (A) The CO pattern of distribution delimits precisely the distinct representations of the contralateral surface, which are congruent with the electrophysiologically defined borders – lips, limbs, trunk and also modules corresponding to individual vibrissae, in homology to the barrel field of small rodents (mouse and rat). (B) Reconstruction of histochemical limits of distinct regions in S1, including cortical modules in the representation of the face. Scale bar: 2 mm. Fl, forelimb; Hl, hindlimb; Ll, lower lip; Tk, trunk; Ul, upper lip; V, vibrissae; LS, lateral sulcus.

FIGURE 7

The pattern of connectivity between S2 and S1. (A) BDA injection (marked with a solid rectangle) in the representation of the forelimb in S2 is connected with its counterpart region in S1, as revealed by a dense focus of projection (dashed rectangle). (B) General reconstruction of a tangential section showing the site of injection of BDA in S2 and its projection to S1. It is possible to identify two foci located rostrally to this region, as well as a small focus near the rhinal fissure, probably area PR. (C) Enlargement of the site of injection in S2 (left) and the focus of projection in S1 (right). Scale bars: A: 5 mm; B,C: 500 μm. LS, lateral sulcus.

FIGURE 8

The pattern of connectivity between S2 and S1. (A) BDA injection in the representation of the forelimb in S2 (arrow). (B,C) Micrograph amplification showing the foci of projection from the region of forelimb representation in S2 to the rostral part of S1 (solid rectangle) and lateral part of S2 (dashed rectangle), respectively (arrows). (D) Electrophysiological mapping of S1 and S2, focusing on the representation of the forelimb, showing the site of injection in S2 (black spot), its projection to S1 (gray spot) and some additional foci located in a rostral region of S1 and area PR. Scale bars: A,D: 5 mm; B,C: 500 μm. LS, lateral sulcus.

FIGURE 9

Schematic diagram representing the general organization of sensory areas and feed forward projections from the forelimb representation in S2. The shaded areas represent projection targets in S1, the motor cortex, and PR. CO modules located in the face area of S1 are represented by hatched areas. Scale bar: 3 mm. Fl, forelimb; Hl, hindlimb; Ll, lower lip; N, nose; Tk, trunk; Ul, upper lip; V, vibrissae; A1, Primary auditory cortex; V1, primary visual cortex; LS, lateral sulcus.