Massive cross-modal cortical plasticity and the emergence of a new cortical area in developmentally blind mammals

Abstract

In the current investigation, the neurophysiological organization of the neocortex was examined in adult animals that were bilaterally enucleated very early in life, before the retino-geniculo-cortical pathway was established. Our results indicate that some aspects of development of cortical fields are not mediated by specific sensory inputs. However, the current study also demonstrates that peripheral innervation plays a large role in the organization of the neocortex, as cortical territories normally involved in visual processing are completely captured by the auditory and somatosensory system. Thus, a large degree of phenotypic variability in cortical organization can be accomplished solely by removing or modifying sensory inputs.

Fig 1.

A comprehensive reconstruction of electrophysiological and architectonic maps of the neocortex in normal (A, case 00-32) and bilaterally enucleated animals (B and C, cases 01-03 and 01-20). (A) The dark purple region indicates V1 as defined both electrophysiologically and architectonically. The light purple indicates extrastriate cortex in which neurons responded exclusively to visual, to visual and auditory, or to visual and somatosensory stimulation. The red and yellow areas correspond to S1 and A1, respectively. Black dots indicate electrode penetrations. (B and C) Red areas correspond to S1, yellow areas correspond to A1, and purple areas correspond to area 17 as architectonically defined. Each dot in A–C represents an electrode penetration. Red dots represent locations at which neurons responded exclusively to somatic stimulation, yellow dots indicate sites at which neurons responded exclusively to auditory stimulation, and red + yellow dots indicate sites at which neurons responded to both somatosensory and auditory stimulation. Recording sites in which neurons did not respond to any type of sensory stimulation are marked as minuses. Thick lines mark architectonic boundaries. Dashed lines represent a portion of the pyriform cortex, included for illustration purposes. In normal animals, S1 contains a complete representation of the contralateral body surface and is coextensive with a darkly myelinated region (Fig. 2). V1 has been well defined in Monodelphis as a complete representation of the contralateral visual hemifield coextensive with a moderately to darkly myelinated region. A1 contains neurons that respond almost exclusively to auditory stimulation, although the tonotopy of this region has not been described in detail in Monodelphis. In the bilaterally enucleated animals, an architectonic area 17 was observed (dark purple), but neurons in this region responded to auditory or auditory + somatosensory stimulation, and the field was substantially smaller than in normal animals (B and C). Also, in bilaterally enucleated animals, a new architectonic area (area X) emerged just lateral to area 17. Neurons in this region responded to auditory + somatosensory stimulation. In cortex lateral to area X, neurons responded to auditory and somatosensory stimulation as well. In the bilateral enucleates, receptive fields for neurons in areas 17, X, MM, A, and CT were mostly on the head, vibrissae, and snout. A1, primary auditory area; CT, caudotemporal area; FM, frontal myelinated area; MM, multimodal cortex; OB, olfactory bulb; PYR, pyriform cortex; S1, primary somatosensory area; V1, primary visual area; V2, second visual area; rostral is to the left and medial is up.

Fig 2.

Cortical myeloarchitecture and cytoarchitecture in normal (A and C, cases 97-41 and 00-30) and bilaterally enucleated (B and D, cases 01-09 and 01-20) Monodelphis. In cortex that has been flattened and stained for myelin, the primary areas are readily defined (A). V1 or area 17 is an area of moderately dense staining for myelin. The primary auditory cortex (A1) is a moderately dense oval just medial to the rhinal sulcus and pyriform cortex, and S1 is a moderately dense region rostral to A1. These regions correspond to electrophysiologically defined regions described in Fig. 1. V2 shares a common border with V1 at the representation of the vertical meridian and can be readily distinguished from V1 as a lightly myelinated region. In the bilaterally enucleated animal (B), S1 and A1 look very similar to the normal animal. Whereas an area 17 can be identified as a small oval at the caudomedial pole of the cortex, it is substantially reduced in size. In these animals, a lightly myelinated area 18 does not adjoin area 17. Rather, a very darkly myelinated area X shares a border with area 17. In normal animals (C), V1 or area 17 has a very densely packed, thickened layer IV. This is in contrast to V2 or area 18, which contains a reduced layer IV. At this mediolateral level, the caudomedial border of S1 is just rostral to V2 and can be identified by its dense granule cell layer. In the bilateral enucleate (D), a small area 17 can also be identified as containing a densely packed, thickened layer IV. The field immediately rostral to area 17, area X, does not look like area 18 in normal animals in that the granular and infragranular layers are indistinct. Cortex immediately rostral to area X at this mediolateral level corresponds to S1. Intensity of myelin stain varied between cases; however, the myeloarchitectonic patterns described here were clearly evident and were consistently observed in each case. In A and B, rostral is to the left and medial is to the top; in C and D, rostral is to the left and dorsal is to the top. OB, olfactory bulb; PYR, pyriform cortex. Other conventions are as in Fig. 1. (Scale bars = 1 mm.)

Fig 3.

The distribution of somatosensory receptive fields in areas 17, X, MM, CT, and A1 in the bilaterally enucleated Monodelphis. Most receptive fields are on the snout, face, head, and vibrissae. The number of recording sites in these areas varied across cases, but the preponderance of receptive fields on these body parts was consistent.