Tonotopic and heterotopic projection systems in physiologically defined auditory cortex.

Combined physiological and connectional studies show significant non-topographic extrinsic projections to frequency-specific domains in the cat auditory cortex. These frequency-mismatched loci in the thalamus, ipsilateral cortex, and commissural system complement the predicted topographic and tonotopic projections. Two tonotopic areas, the primary auditory cortex (AI) and the anterior auditory field (AAF), were electrophysiologically characterized by their frequency organization. Next, either cholera toxin beta subunit or cholera toxin beta subunit gold conjugate was injected into frequency-matched locations in each area to reveal the projection pattern from the thalamus and cortex. Most retrograde labeling was found at tonotopically appropriate locations within a 1 mm-wide strip in the thalamus and a 2-3 mm-wide expanse of cortex (approximately 85%). However, approximately 13-30% of the neurons originated from frequency-mismatched locations far from their predicted positions in thalamic nuclei and cortical areas, respectively. We propose that these heterotopic projections satisfy at least three criteria that may be necessary to support the magnitude and character of plastic changes in physiological studies. First, they are found in the thalamus, ipsilateral and commissural cortex; since this reorganization could arise from any of these routes and may involve each, such projections ought to occur in them. Second, they originate from nuclei and areas with or without tonotopy; it is likely that plasticity is not exclusively shaped by spectral influences and not limited to cochleotopic regions. Finally, the projections are appropriate in magnitude and sign to plausibly support such rearrangements; given the rapidity of some aspects of plastic changes, they should be mediated by substantial existing connections. Alternative roles for these heterotopic projections are also considered.