A Map of Visual Space Induced in Primary Auditory Cortex

Abstract

Maps of sensory surfaces are a fundamental feature of sensory cortical areas of the brain. The relative roles of afferents and targets in forming neocortical maps in higher mammals can be examined in ferrets in which retinal inputs are directed into the auditory pathway. In these animals, the primary auditory cortex contains a systematic representation of the retina (and of visual space) rather than a representation of the cochlea (and of sound frequency). A representation of a two-dimensional sensory epithelium, the retina, in cortex that normally represents a one-dimensional epithelium, the cochlea, suggests that the same cortical area can support different types of maps. Topography in the visual map arises both from thalamocortical projections that are characteristic of the auditory pathway and from patterns of retinal activity that provide the input to the map.

Cross-modal reorganization of callosal connectivity without altering thalamocortical projections

“…We did not find that the pattern of callosal connections in the cross-modal AI resembled that in normal primary visual cortex, where only the neurons representing the visual midline have callosal connections. In fact, a previous mapping study in cross-modal ferrets places the vertical meridian of the visual field in the medial portion of AI (13), the portion that this study shows to be specifically devoid of callosal connections. The right AI in our cross-modal animals probably represents auditory information, especially in animals with smaller unilateral lesions, and the callosal pathway may provide this auditory information to the left AI combined with its visual input from the ipsilateral MGN.…”

“…Providing ferret AI with visual input from early in postnatal development can produce an AI that resembles primary visual cortex very closely in its topography and response properties (13,14). However, the gross pattern of AI's connectivity with other auditory structures remains unaltered, and in particular the thalamocortical pathway remains elongated along the isofrequency axis (12,32).…”

“…The area lateral to AI is the secondary auditory cortical area, AII (32,36,37), and we thus drew the AI͞AII boundary at the apex of the pseudosylvian sulcus. Previous studies have confirmed that AI remains on the crown of the ectosylvian gyrus despite the cross-modal rewiring lesions (11)(12)(13)(14). Patches in many cases extended into AII, and we included these patches in all analyses except as noted.…”

“…Because the manipulation is done peripherally, the modality and thus the pattern of input activity are changed without damaging the thalamocortical pathway carrying the information to cortex (11,12). Under these conditions, AI exhibits receptive field properties usually seen in visual cortex, such as a retinotopic map and orientation-selective visual neurons (13,14). A major question that remains is whether the anomalous visual inputs make use of existing circuitry in AI, or whether they cause active changes in AI's circuitry, organizing it appropriately for processing visual information.…”

Energy, information, detection, and action

“…For example, if retinal projections are redirected to the auditory thalamus in neonatal ferrets, these projections not only activate parts of primary auditory cortex via thalamo-cortical connections but also form a retinotopic map (Roe et al 1990;Sur et al 1988; see also Frost & Metin 1985 for redirected retinal projections to the somatosensory cortex). These visually driven auditory-cortex neurons have typical properties of neurons in the visual cortex, such as orientation and direction selectivity.…”