Evolution off spontaneous activity in the developing rat superior colliculus

Abstract

During the first 10 days after birth in the rat there are a succession of major developmental stages in the retinotectal pathway. During most of this time, the only recordable event in the superior colliculus is spontaneous activity. We studied and characterized this spontaneous activity, hypothesizing that it could play an important role in pathway development. The spontaneous discharges are detectable on postnatal day 5 (P5). After P5, the number of spontaneously active cells per penetration increases up to P10, after which they decrease to adult-like levels by P14-P15. Between P5 and P10, the spontaneous discharges exhibit several patterns of activity, from constant firing to intermittent bursts with periods of quiescence, without any bearing to age. We isolated the retina and superior colliculus by injecting xylocaine onto the optic nerve and found no change in collicular activity. While this suggests that the spontaneous activity in the colliculus is independent of the retina at the ages studied, the opposite experiment, i.e., electrically stimulating the optic nerve, resulted in increased firing by collicular neurons, perhaps via nonclassical synaptic transmission. Finally, we compared interval histograms for spontaneously active cells between P5 and P15. The histograms suggest that at certain ages, spontaneous firing is more regular; moreover, these ages precede major functional advances, e.g., onset of numerous spontaneously firing cells at P6, the first response to optic nerve stimulation at P10, and the first light-evoked response at P12-P13. Our results support the hypothesis that spontaneous activity in the neonatal superior colliculus has a role in development of the retinotectal pathway, but the data also indicate that classical synaptic transmission is not involved.

Retina-Driven Dephosphorylation of the NR2A Subunit Correlates with Faster NMDA Receptor Kinetics at Developing Retinocollicular Synapses

“…For these reasons, we predicted that early light-driven activity in the retina may begin to drive visual neurons of the sSC and initiate the CaN-mediated change. Previous investigations have shown that the photoreceptor-bipolar-ganglion cell pathway is glutamatergic (Itaya et al, 1995;Bansal et al, 2000;Wong et al, 2000). Our data indicate that this pathway can be impaired in the early retina by infiltrating one eye cup with AMPA/KAR and NMDAR antagonists.…”

Developmental Depression of Glutamate Neurotransmission by Chronic Low-Level Activation of NMDA Receptors

“…In the superficial visual layers of the superior colliculus, synaptogenesis can be studied anatomically (Thong and Dreher, 1986;Warton and McCart, 1989;Contamina and Boada, 1992;Colonnese and Constantine-Paton, 2001) and physiologically (Itaya et al, 1995;Binns and Salt, 1997;Fortin et al, 1999) because of the direct and dominant innervation from the retina and visual cortex and the synchronization of synaptic development (Shi et al, 1997Aamodt et al, 2000). Previously we reported that chronic application of low levels of NMDA to the sSC at P8 upregulates GABA A receptor-mediated synaptic activity at P12, 5 d before this increase would occur during normal development.…”

Homeostatic synaptic plasticity in developing spinal networks driven by excitatory GABAergic currents

“…SNA is expressed in the spinal cord, retina, hippocampus, brain stem, superior colliculus, and others, shortly after synaptic connections first form, (Gummer and Mark, 1994; Fortin et al, 1995; Itaya et al, 1995; Lippe, 1995; Feller, 1999; Ho and Waite, 1999; O’Donovan, 1999; Wong, 1999; Ben-Ari, 2001). SNA exists as episodic bursts of spiking activity that last for seconds and are followed by longer lasting quiescent periods, as shown in Figure 1 (muscle nerve recordings in chick embryo spinal preparation).…”