Functional organization of the electroreceptive midbrain in an elasmobranch (Platyrhinoidis triseriata)

Abstract

The response properties of 322 single units in the electroreceptive midbrain (lateral mesencephalic nucleus, LMN) of the thornback ray, Platyrhinoidis triseriata, were studied using uniform and local electric fields. Tactile, visual, or auditory stimuli were also presented to test for multimodality. Most LMN electrosensory units (81%) are silent in the absence of stimulation. Those with spontaneous activity fired irregularly at 0.5 to 5 impulses/s, the lower values being more common. Two units had firing rates greater than 10/s. Midbrain electrosensory units are largely phasic, responding with one or a few spikes per stimulus onset or offset or both, but the adaptation characteristics of some neurons are complex. The same neuron can exhibit phasic or phasic-tonic responses, depending upon orientation of the electric field. Tonic units without any initial phasic over-shoot were not recorded. Even the phasic-tonic units adapt to a step stimulus within several seconds. Unit thresholds are generally lower than 0.3 microV/cm, the weakest stimulus delivered, although thresholds as high as 5 microV/cm were recorded, Neuronal responses reach a maximum, with few exceptions, at 100 microV/cm and decrease rapidly at higher intensities. LMN neurons are highly sensitive to stimulus repetition rates: most responded to frequencies of 5 pulses/s or less; none responded to rates greater than 10/s. Three distinct response patterns are recognized. Best frequencies in response to sinusoidal stimuli range from 0.2 Hz (the lowest frequency delivered) to 4 Hz. Responses decrease rapidly at 8 Hz or greater, and no units responded to frequencies greater than 32 Hz. Most LMN neurons have small, well defined excitatory electroreceptive fields (RFs) exhibiting no surround inhibition, at least as detectable by methods employed here. Seventy-eight percent of units recorded had RFs restricted to the ventral surface: of these, 98% were contralateral. The remaining 22% of units had disjunct dorsal and ventral receptive fields. Electrosensory RFs on the ventral surface are somatotopically organized. Anterior, middle, and posterior body surfaces are mapped at the rostral, middle, and caudal levels, respectively, of the contralateral LMN. The lateral, middle, and medial body are mapped at medial, middle, and lateral levels of the nucleus. Moreover, the RFs of all units isolated in a given dorsoventral electrode track are nearly superimposable. About 40% of LMN, measured from the dorsal surface, is devoted to input from ventral electroreceptors located in a small region rostral and lateral to the mouth.(ABSTRACT TRUNCATED AT 400 WORDS)

Organization of Major Telencephalic Pathways in an Elasmobranch, the Thornback Ray <i>Platyrhinoidis triseriata</i>

“…This projection was also reported by Luiten [1981b], Bodznick and Northcutt [1984], and Fiebig and Bleckmann [1989]. It might be part of an ascending electrosensory pathway [Schweitzer, 1983[Schweitzer, , 1986Bodznick and Northcutt, 1984]. In our study, only a few cells were labeled in those dorsal thalamic areas that may correspond to the lateral geniculate and ventral optic nucleus of Luiten [1981b].…”

Medullary and Mesencephalic Pathways and Connections of Lateral Line Neurons of the Spiny Dogfish <i>Squalus acanthias</i>

“…Boord and Northcutt [1982] were unable to trace secondary lateral line projections to it but showed that it receives electrosensory afferents from the more caudally situ ated lateral subdivision [Boord and Northcutt, 1983]. Schweitzer [ 1986], using electrophysiological methods in the thornback guitar fish, presents evidence that the anterior and lateral subdivisions represent a single somatotopic map of the electrosensory body surface and suggests that they are parts of the same nucleus. Bleckmann et al [1987] recorded responses to both electrical and mechanical stimuli from cells of the an terior nucleus in the thornback guitar fish and do not believe that it is a rostral extension of the lateral nuc leus.…”

Central Organization of Wave Localization in the Clawed Frog, <i>Xenopus laevis</i>

“…The transverse sections are shown from behind, so that a left-side lesion is seen on the left side of the sections and vice versa. h DCBA demonstrated a topological correlation between stim ulus direction and neural processing in the midbrain of anamniotes in hearing [Pettigrew et al, 1978[Pettigrew et al, , 1981, the somatosensory system [Comer and Grobstein, 1981b], electroreception [Scheich and Maler, 1976;Knudsen, 1977Knudsen, , 1978Bastian, 1982;Schweitzer, 1986], and the mechanoreceptive lateral line [Knud sen, 1977;Zittlau et al, 1986]. Behavioral validation for the functional significance of these results, how ever, is lacking.…”