Influence of the tectal zone on the distribution of synaptic boutons in the brainstem of goldfish

Abstract

This study investigated whether the topographic differences in the functional properties of the tectal motor map of goldfish are related to particular patterns of connections with downstream structures. With this aim, the distribution of synaptic boutons in the mesencephalic and rhombencephalic structures was studied after discrete injections of the tracer biotinylated dextran amine were placed at separate sites along the tectal anteroposterior axis. Irrespective of the location of the injection site, the boutons were more abundant in the mesencephalon than in the rhombencephalon, and they were located chiefly ipsilaterally all throughout the brainstem. In the mesencephalon, the boutons were found in its ventrolateral reticular formation and, to a lesser extent, in the nucleus of the medial longitudinal fasciculus, the oculomotor and isthmi nuclei, and the torus semicircularis. In the mesencephalic reticular formation, the bouton location was distributed topographically with respect to the injection site. Terminals were also observed in the nucleus of the medial longitudinal fasciculus after injections into anteromedial or middle tectal zones. In the oculomotor nucleus, boutons were present exclusively in the case of the anteromedial injection. In the rhombencephalon, most boutons were found in the superior reticular formation, and their number decreased in the medial and inferior reticular formations. A topographic distribution could be observed within the superior reticular formation, although its density was attenuated compared with that observed in the mesencephalic reticular formation. The domains of synaptic endings on the ipsilateral side were different from those on the contralateral side: The ipsilateral synaptic endings were located more medially. Finally, a few boutons were also found in the vestibulocerebellar area on either the ipsilateral or the contralateral side, depending on the injection site. From these data, the authors conclude that, in goldfish, irrespective of the tectal injection site, the endings are in similar nuclei in the brainstem; however, the distribution of synaptic boutons within such nuclei can be related to the functional properties of each tectal zone.

Afferent connectivity to different functional zones of the optic tectum in goldfish

“…A reciprocal connectivity of the torus semicircularis with the optic tectum has been thoroughly reported previously in fish (Grover & Sharma, 1979, 1981Luiten, 1981;Fiebig et al, 1983;Schlussman et al, 1990;Herrero et al, 1998a). In nonelectroreceptive teleosts, the torus semicircularis is involved in processing the acoustic and lateral line signals (Lu & Fay, 1993;Wubbels & Schellart, 1997;Meek & Nieuwenhuys, 1998).…”

“…However, the approach of these works to tectal connectivity did not fully allow for differences in the characteristics by which different tectal zones evoke movements and the possibility that each zone could maintain a particular wiring in its efferents and afferents with distinct brain structures. Indeed, recent studies have shown that tectal efferent connectivities with the mesencephalic and rhombencephalic reticular formation are different depending on the functional properties of each tectal zone (Herrero et al, 1998a;Moschovakis et al, 1998;Perez-Perez et al, 2000). Furthermore, morphological studies of afferents to different tectal zones, which were not functionally identified, showed both differences in the pattern of projections to the rostral and caudal tectum (Grover & Sharma, 1981) and a topographical organization of afferents from the nucleus isthmi to the tectum (Sakamoto et al, 1981;Dunn-Meynell & Sharma, 1984).…”

Visual Prey Capture in Larval Zebrafish Is Controlled by Identified Reticulospinal Neurons Downstream of the Tectum

“…MeLr and MeLc extend elaborate dendrites into the deeper layers of the tectum. Here, the cell bodies of tectofugal projection neurons are situated (Meek and Schellart, 1978;Nguyen et al, 1999), which, in other teleosts, have been reported to send a predominantly ipsilateral and excitatory projection to the nMLF (Bosch and Paul, 1993;Herrero et al, 1998a;Niida et al, 1998;Zompa and Dubuc 1998a,b;Isa and Sasaki, 2002;Torres et al, 2002;Perez-Perez et al, 2003). MeLr and MeLc extend axons into the spinal cord, arborizing predominantly in its rostral segments, in which their axon terminals colocalize with motor neurons and interneurons .…”

Integrating Brain and Biomechanical Models—A New Paradigm for Understanding Neuro-muscular Control

“…As we modeled a left eye, this actuates the lateral rectus muscle. The exponential rise of Equation (29) (for experimental evidence, see Figures 7, 8 of Herrero et al, 1998 ) is seen in the r direction; as r increases, so the connection strength to the SBG channel rises exponentially. The connection strength is greatest along the center line, for a value of ϕ which corresponds to a purely leftward movement.…”

“…The spatial aspect of the transform is thought to be implemented by a weight-mapping (Arai et al, 1994 ; Tabareau et al, 2007 ). Although there is no definitive experimental proof for such a mapping, there exists evidence for spatially variable synapse density (Herrero et al, 1998 ; Moschovakis et al, 1998 ) and connection density (Grantyn et al, 2002 ) and we therefore adopt the idea. Arai and co-workers trained a 20 by 20 neural network model of the superior colliculus to discover the weight map under the assumption of 2D Gaussian activation profiles (Arai et al, 1994 )—that is, they assumed that the activity in superior colliculus for any saccade was a size-invariant 2D Gaussian hill of activity.…”