Segregation of electro- and mechanoreceptive inputs to the elasmobranch medulla

The anterior lateral line nerve of the thornback ray consists of fibers that innervate head electroreceptive ampullary organs and mechanoreceptive neuromasts. As the anterior lateral line nerve enters the medulla it divides into dorsal and ventral roots. Single unit responses of dorsal root fibers to electric field and mechanical stimuli indicate that the dorsal root consists only of ampullary fibers, whereas the ventral root consists only of mechanoreceptive fibers. The dorsal and ventral roots of the anterior lateral line nerve terminate in the dorsal and medial octavolateralis nuclei respectively, indicating that the dorsal nucleus is the primary electroreceptive nucleus of the elasmobranch medulla and the medial nucleus is the mechanoreceptive nucleus. Averaged evoked potential responses to electric field stimuli could be recorded from the dorsal but not the medial nucleus, further evidence that the dorsal nucleus is the electroreceptive nucleus. A second evoked response to electric field stimuli was elicited from the lateral reticular nucleus, suggesting that the reticular formation may be a secondary target of efferents of the dorsal octavolateralis nucleus. A dorsal octavo-lateralis nucleus exists not only in elasmobranchs, but also in agnathan, chondrostean, dipnoan, and crossopterygian fishes, suggesting that all of these taxa are also electroreceptive.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/23168/1/0000093.pd

An electrosensory area in the telencephalon of the little skate, Raja erinacea

On the basis of evoked potential and multiple unit responses we identified a pallial electrosensory area that extends throughout the central one-third of the skate telencephalon. This electrosensory area coincides in its mediolateral and rostrocaudal extent with an area of visual responsiveness. Throughout the area peak visual activity is 250-500 [mu]m superficial to the maximum electrosensory responses. However, both electrosensory and visual areas appear to be located within the same pallial cell group. The depth and proximity of this pallial area to the lateral ventricle and medial forebrain bundle suggest that it is a subdivision of the medial pallium. Injection of HRP into the area from a glass microelectrode following recordings revealed retrogradely labeled cells in 3 separate diencephalic nuclei, the largest of which, the lateral posterior nucleus, also is responsive to electrosensory stimuli.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/24842/1/0000268.pd

Morphological development of the dorsal hindbrain in an elasmobranch fish (Leucoraja erinacea)

Abstract The developmental anatomy of the dorsal hindbrain in an elasmobranch fish, Leucoraja erinacea, is described. We focus on the cerebellum, which is a synapomorphy for gnathostomes. Cerebellar development in L. erinacea, a representative of the most basal gnathostome lineage, may be a proxy for the ancestral state of cerebellar development. We also focus on sensory processing regions termed ‘cerebellum-like’ structures due to common anatomical and physiological features with the cerebellum. These structures may be considered generatively homologous if they share common developmental features. To test this hypothesis, the morphological development of the cerebellum and cerebellum-like structures must first be described. Of particular importance is the development of common features, such as the molecular layer, which is the defining characteristic of these structures. The molecular layers of the cerebellum and cerebellum-like structures are supplied with parallel fiber axons from distinct granule cell populations. These are the lateral granule mass, the dorsal granular ridge, the medial granule mass, and the granular eminences of the cerebellum. Cerebellar and cerebellar-like development in L. erinacea is similar to development in other elasmobranchs. The temporal order in which these granule cell populations develop suggests an evolutionary history of duplication or expansion of an existing developmental event

A cerebellum-like circuit in the lateral line system of fish cancels mechanosensory input associated with its own movements

Author Posting. © Company of Biologists, 2020. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 223 (2020): jeb.204438, doi:10.1242/jeb.204438.An animal's own movement exerts a profound impact on sensory input to its nervous system. Peripheral sensory receptors do not distinguish externally generated stimuli from stimuli generated by an animal's own behavior (reafference) – although the animal often must. One way that nervous systems can solve this problem is to provide movement-related signals (copies of motor commands and sensory feedback) to sensory systems, which can then be used to generate predictions that oppose or cancel out sensory responses to reafference. Here, we studied the use of movement-related signals to generate sensory predictions in the lateral line medial octavolateralis nucleus (MON) of the little skate. In the MON, mechanoreceptive afferents synapse on output neurons that also receive movement-related signals from central sources, via a granule cell parallel fiber system. This parallel fiber system organization is characteristic of a set of so-called cerebellum-like structures. Cerebellum-like structures have been shown to support predictive cancellation of reafference in the electrosensory systems of fish and the auditory system of mice. Here, we provide evidence that the parallel fiber system in the MON can generate predictions that are negative images of (and therefore cancel) sensory input associated with respiratory and fin movements. The MON, found in most aquatic vertebrates, is probably one of the most primitive cerebellum-like structures and a starting point for cerebellar evolution. The results of this study contribute to a growing body of work that uses an evolutionary perspective on the vertebrate cerebellum to understand its functional diversity in animal behavior.This work was supported by National Science Foundation (NSF) and Wesleyan University grants to D.B. Funding for K.E.P. while performing these experiments came in part from a grant from the HHMI Hughes V award for undergraduate education to Wesleyan University (52005211) in the form of a summer research fellowship. A.K. was supported in part by an NSF-REU Award (1659604) and a Wesleyan University Summer Research Fellowship. K.E.P. is currently supported through funding from the Simons Society of Fellows as a Junior Fellow.2021-01-1

Multiple behavior-specific cancellation signals contribute to suppressing predictable sensory reafference in a cerebellum-like structure

Author Posting. © Company of Biologists, 2021. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 224(7), (2021): jeb.240143, https://doi.org/10.1242/jeb.240143.Movement induces sensory stimulation of an animal's own sensory receptors, termed reafference. With a few exceptions, notably vestibular and proprioception, this reafference is unwanted sensory noise and must be selectively filtered in order to detect relevant external sensory signals. In the cerebellum-like electrosensory nucleus of elasmobranch fish, an adaptive filter preserves novel signals by generating cancellation signals that suppress predictable reafference. A parallel fiber network supplies the principal Purkinje-like neurons (called ascending efferent neurons, AENs) with behavior-associated internal reference signals, including motor corollary discharge and sensory feedback, from which predictive cancellation signals are formed. How distinct behavior-specific cancellation signals interact within AENs when multiple behaviors co-occur and produce complex, changing patterns of reafference is unknown. Here, we show that when multiple streams of internal reference signals are available, cancellation signals form that are specific to parallel fiber inputs temporally correlated with, and therefore predictive of, sensory reafference. A single AEN has the capacity to form more than one cancellation signal, and AENs form multiple cancellation signals simultaneously and modify them independently during co-occurring behaviors. Cancellation signals update incrementally during continuous behaviors, as well as episodic bouts of behavior that last minutes to hours. Finally, individual AENs, independently of their neighbors, form unique AEN-specific cancellation signals that depend on the particular sensory reafferent input it receives. Together, these results demonstrate the capacity of the adaptive filter to utilize multiple cancellation signals to suppress dynamic patterns of reafference arising from complex co-occurring and intermittently performed behaviors.This work was supported by National Science Foundation (NSF) and Wesleyan University grants to D.B. N.Y.L. was supported by Wesleyan University grants, a Freeman Asian Scholarship, and a Howard Hughes Medical Institute award for undergraduate summer research.2022-04-1