Optic nerve-dependent changes in adult frog tectal cell phenotypes

Abstract

Optic nerve activity helps determine the placement of retinal ganglion cell terminals in the optic tectum of the frog. We investigated whether the presence of this nerve might also influence a characteristic of its target structure, neurotransmitter biosynthesis. We performed unilateral optic nerve transections on adult animals and assayed the percent and intensity of substance P‐ and serotoninlike immunoreactive (SP‐ir and 5‐HT‐ir, respectively) cells in the deafferented and afferented tectal lobes. Regeneration of the optic nerve was prevented. The percent of SP‐ir cells in the afferented tectal lobes was significantly less than that in the deafferented ones either 6 weeks or 5 months following optic nerve lesion. Comparison to normal animals indicated that the change in SP‐ir expression was due to a decrease in the percent of immunoreactive cells in the afferented tecta ipsilateral to the optic nerve lesion. The serotoninlike immunoreactivity of tectal cells was also significantly different in the two lobes following optic nerve lesions. This difference resulted from an increase in the percent of 5‐HT‐ir cells in the deafferented tectum. In addition, the intensity of 5‐HT‐ir cells in the deafferented lobe was significantly greater than in the afferented one. The staining intensity of SP‐ir cells underwent only a transient, relative decrease in the deafferented tectum. We conclude that the optic nerve does regulate substance P and serotonin expression in the tectum, but that this regulation likely occurs through different pathways. © 1996 John Wiley & Sons, Inc.

Neurotrophins, but not depolarization, regulate substance P expression in the developing optic tectum

“…Consistent with the idea that this cholinergic pathway is activated by glutamatergic depolarization of tectal cells is the observation that chronically blocking tectal non-NMDA receptors with CNQX produces a decrease in SP-ir cells in the untreated lobe. This decrease mimics that seen in the afferented lobe in response to optic nerve transection (Liu and Debski, 1996).…”

“…The size of this population is dependent on the presence of the optic nerve. Unilateral optic nerve transection causes a decrease in SP-ir tectal cells in both the adult and developing systems, but in the former instance this decrease occurs in the afferented tectal lobe (Liu and Debski, 1996), while in the latter it happens in the deafferented lobe (Tu and Debski, 1999). Although direct optic nerve input to each tectal lobe originates almost entirely from the contralateral retina (Singman and Scalia, 1990), pathways exist within the brain that relay information from one tectal lobe to the other (Gruberg and Udin, 1978;Grobstein and Comer, 1983).…”

Activity-Dependent Regulation of Substance P Expression and Topographic Map Maintenance by a Cholinergic Pathway

“…Our previous work demonstrated that transection of the optic nerve causes a decrease in SP-IR cells in the innervated tectal lobe, whereas SP expression in the deafferented lobe is unaffected (Liu and Debski, 1996). Because each tectal lobe receives direct retinal input almost exclusively from the contralateral eye (Singman and Scalia, 1990), this result suggested to us that SP expression was being regulated by activity that was relayed between the two tectal lobes.…”

“…SP is expressed in a subpopulation of tectal neurons found exclusively in layer 6 ( Kuljis and Karten, 1982). Our previous work has shown that unilateral optic nerve transection decreases the percentage of SP-IR cells in the afferented tectum but leaves the deafferented tectum unchanged (Liu and Debski, 1996). This suggests that SP expression in tectal cells is regulated by activity that is relayed from one tectal lobe to the other.…”

“…The visual system of the frog provides an opportunity to examine how in vivo depolarizing activity changes SP expression. Previously we have found that optic nerve transection decreases SP expression in neurons in the tectal lobe still receiving visual input (Liu and Debski, 1996). The known pharmacology of the frog visual pathways (Desan et al, 1987;Hickmott and Constantine-Paton, 1993), combined with a chronic drug release technique (Cline et al, 1987), allows us to selectively block activity evoked by signals from different tectal afferents.…”