Intracellular recording and simultaneous intracellular dye injection techniques were applied to deafferented trigeminal second-order neurons in the brainstem to determine how altered peripheral connections might change the structure and function of brainstem neurons. With these techniques, we were able to determine whether the structure of a brainstem cell reflects the nature of its inputs from the peripheral nervous system, and whether altered first-order response properties and passed on to higher-order trigeminal neurons. To date, 54 adult second-order cells have been intracellularly labeled and studied by electrophysiology, after infraorbital nerve section at birth. Some of these deafferented cells had apparently normal structure, yet unusual response properties. For example, one cell which sent its axon to the cerebellum responded to deflection of all of the whiskers and small hairs on the left side of the head. These properties are never seen in normal trigeminal second-order cells that send their axons to the cerebellum. Moreover, reconstruction of the cell's dendritic processes indicated that they were no more widespread than that for similar neurons in normal rats. Normally these cells have a much more restricted receptive field on the face (i.e., 1 or 2 whiskers). Thus, dendritic reorganization is probably not responsible for the development of this novel receptive field. Similarly, deafferented trigeminal second-order neurons that sent their axons to the thalamus often exhibited widespread receptive fields that included an unusual combination of receptor surfaces, yet their structure appeared normal. These functional properties may, therefore, reflect alterations in first-order inputs, unmasking of previously ineffective inputs, or reorganization of other systems which normally project into the trigeminal brainstem region. The data suggest that, for these neurons, second-order cell structure does not necessarily reflect the nature of first-order inputs, though the latter certainly contribute to second-order response properties.
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