Pattern formation by retinal afferents in the ferret lateral geniculate nucleus: Developmental segregation and the role of N‐methyl‐D‐aspartate receptors

Abstract

The projection from the retina to the lateral geniculate nucleus (LGN) in ferrets segregates during development into eye‐specific layers and ON/OFF sublayers. The projection pattern and the morphology of single axons was examined at several postnatal ages. The axons progress from a simple, sparsely branched morphology at birth to crude arbors at postnatal day 7 (P7). At P14–P15, axons have terminal arbors that span one eye‐specific layer. By P19–P21, retinal afferents in the A layers have segregated into inner and outer sublaminae that correspond to ON‐ and OFF‐center cells. Sublaminae form mainly by directed growth of terminal arbors in appropriately positioned regions of the LGN, along with elimination of extraneous branches in inappropriate regions. From P28 to P35, the LGN assumes an adult‐like shape, and retinogeniculate axons form terminal boutons on branch endings. During the period between P14 and P21, when retinogeniculate axons segregate into ON/OFF sublaminae, N‐methyl‐D‐aspartate (NMDA) receptors were blocked with chronic infusion of specific antagonists into the LGN. NMDA receptor blockade prevents the retinal afferent segregation into ON/OFF sublaminae. Some individual retinogeniculate axons have arbors that are not restricted appropriately, and most are restricted in size but are located inappropriately within the eye‐specific laminae. Thus, NMDA receptor blockade prevents the positioning of retinogeniculate arbors that lead to the formation of ON/OFF sublaminae in the LGN. These results indicate that the activity of postsynaptic cells, and the activation of NMDA receptors in particular, can influence significantly the patterning of inputs and the structure of presynaptic afferents during development. J. Comp. Neurol. 411:327–345, 1999. © 1999 Wiley‐Liss, Inc.

Deletion of voltage‐gated channel affects glomerular refinement and odorant receptor expression in the mouse olfactory system

“…In the visual system, refinement of the topographic map is thought to require the participation of postsynaptic cells, such that correlated activity in presynaptic neurons results in the release of factors that subsequently modify the presynaptic arbors (Cramer and Sur, 1995; Fitzsimonds and Poo, 1998). In particular, blockade of the N-methyl-D-aspartate (NMDA) receptor that alters activity of postsynaptic cells significantly influences the patterning of inputs and the structure of presynaptic afferents in the visual system (Hahm et al, 1999). It might be possible that a similar mechanism may exist in the olfactory system to refine the glomeruli toward a homogeneous entity of similar axons.…”

NMDA Receptor Currents Suppress Synapse Formation on Sprouting AxonsIn Vivo

“…One prevalent theory is that coordinated patterns of activity facilitate afferent stabilization by activating postsynaptic receptors Katz and Shatz, 1996). However, despite disruption of topography or lamination, retinal axons can elaborate in the absence of presynaptic action potentials (O'Leary and Cowan, 1983;Thompson and Holt, 1989;Cook et al, 1999) or postsynaptic NMDAR activity Hahm et al, 1999). Glutamatergic synaptic function also develops relatively normally in the absence of NMDAR activity (Zhu and Malinow, 2002;Colonnese et al, 2003).…”

“…However, after NMDAR blockade, the retinotopic map formed by the contralateral retina in the sSC of rats (Simon et al, 1992) and the tectum of frogs (Cline and Constantine-Paton, 1989) is normal in terms of gross topography and density of arbors; only the removal of topographically inappropriate arbors is prevented. In the ferret lateral geniculate nucleus, retinal ganglion cell (RGC) axons target correct eye-specific lamina and arborize without NMDAR activity, but they fail to restrict their branching to on-and offspecific sublaminar regions (Hahm et al, 1999). In chick tectum, the elimination of ipsilateral RGC axons is reduced by NMDAR blockade (Ernst et al, 1999).…”

Spatial and Temporal Properties of Visual Responses in the Thalamus of the Developing Ferret

“…In the period before eye opening, neuronal connections are changing throughout the ferret primary visual pathway, and many of these changes are thought to be modulated by activity. For instance, retinal afferents in the dLGN segregate first into eyespecific territories (Linden et al, 1981) and subsequently into On and Off zones (Hahm et al, 1999). In the period immediately after the onset of visual responsiveness, neuronal connections continue to change and refine in the ferret primary visual pathway.…”