Shared versus Specialized Glycinergic Spinal Interneurons in Axial Motor Circuits of Larval Zebrafish

Abstract

The neuronal networks in spinal cord can produce a diverse array of motor behaviors. In aquatic vertebrates such as fishes and tadpoles, these include escape behaviors, swimming across a range of speeds, and struggling. We addressed the question of whether these behaviors are accomplished by a shared set of spinal interneurons activated in different patterns or, instead, involve specialized spinal interneurons that may shape the motor output to produce particular behaviors. We used larval zebrafish because they are capable of several distinct axial motor behaviors using a common periphery and a relatively small set of spinal neurons, easing the task of exploring the extent to which cell types are specialized for particular motor patterns. We performed targeted in vivo whole-cell patch recordings in 3 d post fertilization larvae to reveal the activity pattern of four commissural glycinergic interneuron types during escape, swimming and struggling behaviors. While some neuronal classes were shared among different motor patterns, we found others that were active only during a single one. These specialized neurons had morphological and functional properties consistent with a role in shaping key features of the motor behavior in which they were active. Our results, in combination with other evidence from excitatory interneurons, support the idea that patterns of activity in a core network of shared spinal neurons may be shaped by more specialized interneurons to produce an assortment of motor behaviors.

Functional Role of a Specialized Class of Spinal Commissural Inhibitory Neurons during Fast Escapes in Zebrafish

“…At least for CoLos, however, this is not the case: CoLos were never active during swimming. The same conclusion was reported recently by Liao and Fetcho (2008), in which the authors further showed that CoLos were not active during struggling, a very strong but slower movement. A likely reason why the spinal cord contains this specialized class of neurons is that the speeds required for escapes and swimming/struggling differ greatly; inhibition mediated by the commissural interneurons without CoLos would not be fast enough for escapes.…”

“…While this paper was in preparation, Liao and Fetcho (2008) independently identified CoLos and examined their firing patterns during three types of behaviors: swimming, struggling and escape. They reported that the firing activity of CoLos was only observed during escapes.…”

Initiation of Locomotion in Adult Zebrafish

“…Unraveling the intrinsic function of the spinal network requires model systems that are accessible for the combination of molecular and genetic tools together with electrophysiology. In this regard, the zebrafish at early developmental stages has emerged as an attractive system that already enabled some of the neuronal components for swimming and escape behavior (Drapeau et al, 2002;Kimura et al, 2006;McLean et al, 2007;Fetcho et al, 2008;Liao and Fetcho, 2008;McLean et al, 2008;Satou et al, 2009;Fetcho and McLean, 2010). These studies need to be extended from larval to juvenile and adult stages to determine whether there is further refinement of the neuronal components of the locomotor circuit that is associated with a change in the swimming behavior, from larval burst swimming to the adult pattern of slow, steady swimming movements and the organization of the motor column (van Raamsdonk et important is how the neural mechanisms responsible for interactions between the swimming and escape circuits are adapted as the animal's shape and speed of locomotion changes during development.…”

“…These different repertoires of motor patterns are thought to result from discrete and interacting circuits that can be selectively activated by descending inputs from the brain. Studies in larval zebrafish have begun to explore the role of different interneuron types during escape and swimming as well as their activation by descending neurons (e.g., Mauthner cells) (Gahtan et al, 2002;Liao and Fetcho, 2008;Satou et al, 2009). Recently, it has been shown that there is a topographic order of recruitment of interneurons and motoneurons that match their order of development (McLean et al, 2007El Manira and Grillner, 2008;McLean and Fetcho, 2009;Roberts et al, 2010).…”

Generation of Multiple Classes of V0 Neurons in Zebrafish Spinal Cord: Progenitor Heterogeneity and Temporal Control of Neuronal Diversity

“…Therefore, glycinergic CoBLs are likely to be included among what we have designated as glycinergic V0-iBs. Glycinergic CoBLs were shown to fire in phase with motoneurons located nearby during swimming, and thus, they are suggested to play a role in left-right reciprocal inhibition of body movements during swimming (Liao and Fetcho, 2008). A study in dbx1 mutant mice suggests that V0 inhibitory neurons in mammals play an important role in coordinating movements across the left and right sides of the body (Lanuza et al, 2004).…”