Functional properties of regenerated optic axons terminating in the primary olfactory cortex

Abstract When the optic nerve of Rana pipiens is cut and deflected into the telencephalon, the regenerating fibers terminate selectively in the superficial neuropil of the primary olfactory cortex. These redirected fibers and their terminals on the dendrites of the cortical cells appear normal by LM and EM criteria. Electrical recording, done 2–16 months after surgery, shows visually evoked activity in the superficial neuropil (Layer I) of the olfactory cortex, and visually excited responses in the deep cortical cell layer (Layer II). In the normal frog, the electrical activity seen in the neuropil of the olfactory cortex consists of small transients about 2–3 × the noise level of the electrode contact. These occur spontaneously and are also excited by puffs of air to the nose. There is no such excitation by visual stimuli. Larger initially negative spikes cell above noise level are recorded in the cell layer next to the ependymal surface, and these are also spontaneous, or excited by puffs of air to the nose, but not by visual stimuli. In the operated frog, the small transients in the neuropil appear and are excited by the puffs of air and by visual stimuli. Similarly the responses in the cell layer are excited by both sorts of stimuli. But new types of electrical signals appear in the neuropil; they are driven only by visual stimuli presented to the affected eye. These are very large transients of the kind found in the tectal neuropil and have the two characteristic shapes which were classified as B and C types in the tectum. Such large transients are never seen in the neuropil of the olfactory cortex in normal frogs. The receptive fields of the small visually driven transients in the neuropil are not easy to make out because the signal levels are so close to the noise level that different units cannot be reliably distinguished from each other. But the receptive fields of the much larger B and C type unit responses are as easy to classify and plot as they are in tectum, even though on the average they are only about 2 3 as large as in tectum. The single-unit receptive fields belong to one or another of the several types of retinal ganglion cell classes distinguished in optic-nerve recordings. Four of the major classes normally project to the tectum and a fifth projects to the lateral geniculate complex. But all five are present in the ectopic projection to the olfactory cortex. The various classes of ganglion cell operations are only crudely stratifid in the olfactory cortex. The classes mediated by unmyelinated fibers (Classes I and II) are represented superficially in the neuropil; the myelinated contingent (Classes III and IV) are often found deeper. But a strict ordering by depth as seen in the tectum is not found in the cortex. In some of the operated frogs, several large, distinct B and C units, discriminable by size and shape, can be recorded at a single electrode position in the neuropil. Then both the single-unit receptive field (SURF) of each unit can be classified and plotted and also the multi-unit receptive field (MURF) of their distribution in the visual field. However, the MURFs are not densely filled with single units, as they are in the tectum, and they subtend much wider areas in the visual field. Generally, the SURFs are also not related systematically to the position of the recording electrode on the cortical surface. Thus, there is no finely ordered retinotopic map in the olfactory cortex. However, almost all the B and C units responded only to stimuli presented (monocularly) in the frontal part of binocular region of the visual field.