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

Summary

• 1. 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.

• 2. 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.

• 3. 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 overshoot were not recorded. Even the phasic-tonic units adapt to a step stimulus within several seconds.

• 4. Unit thresholds are generally lower than 0.3 μV/cm, the weakest stimulus delivered, although thresholds as high as 5μV/cm were recorded. Neuronal responses reach a maximum, with few exceptions, at 100 μV/cm and decrease rapidly at higher intensities.

• 5. 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.

• 6. 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.

• 7. 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.

• 8. 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.

• 9. The rostrocaudal extent of the somatotopic map includes regions of the neuraxis previously divided into 2 nuclei of the lateral mesencephalic complex, the anterior nucleus (AN) anteriorly and lateral nucleus (LMN) caudally. The single, unfractured somatotopic map reported here is continuous across the boundary of these two regions. This suggests that AN may not be a distinct nucleus but rather a rostral extension of LMN.

• 10. LMN neurons are sensitive to the orientation of a uniform electric field. Maximum and minimum responses can be recorded at orientations separated by just 30°. Single unit best orientations are largely a function of the orientation of ampullary canals from which a unit receives input.

• 11. The majority of LMN electrosensory units are bimodal, responding vigorously to a camel-hair brush applied gently to the skin. This midbrain mechanosensitivity apparently is not mediated by the ampullae of Lorenzini since tactile stimuli adequate in the midbrain do not excite medullary electrosensory neurons. Mechanosensory minimum RFs are generally larger than but invariably overlap with electrosensory RFs. The somatotopic maps of the 2 modalities are congruent. Cross-modality interactions in bimodal units were observed and will be discussed.