Filial imprinting in domestic chicks is associated with spine pruning in the associative area, dorsocaudal neostriatum

Abstract

Juvenile emotionally modulated learning events are fundamental for the normal development of socio-emotional competence and intellectual capabilities. Filial imprinting in the domestic chick provides a suitable model to investigate the neural mechanisms underlying such juvenile learning events. The forebrain area dorsocaudal neostriatum (Ndc), a multimodal integration area and presumed equivalent to mammalian parietotemporal association cortices, has been shown to be critically involved in this learning process. We investigated whether filial imprinting is associated with changes of synaptic connectivity in the Ndc. Quantitative measurements of spine densities of a large neuron type in the Ndc revealed a massive pruning of spine synapses after filial imprinting. Compared with 7-day-old naive control chicks, imprinted chicks displayed significantly lower spine frequencies on all dendritic segments. Since the average length of the dendritic segments did not change during imprinting, these results can be interpreted as a reduction of the absolute number of spine synapses on this neuron type. In a control region, the primary sensory forebrain area ectostriatum, spine density and dendritic length remained unchanged. These results indicate that synaptic pruning may represent a mechanism of selective synaptic reorganization in higher associative forebrain areas as a fundamental feature of juvenile learning events.

The inhibition of acquired fear

“…One of these events could well be the pruning of axonal and dendritic ramifications, which is inhibited by AP5 and CaMKII inhibitors (Zou and Cline, 1999) and has been shown to underlie the formation of very strong and lasting memories, such as imprinting in birds (Bock and Braun, 1999b). The synaptic elimination process that underlies imprinting is inhibited by AP5 (Bock and Braun, 1999a).…”

Lateral magnocellular nucleus of the anterior neostriatum (LMAN) in the zebra finch: Neuronal connectivity and the emergence of sex differences in cell morphology

“…Our findings of overproduction and subsequent pruning of neural connections are consistent with the synapse selection hypothesis of Changeux and Danchin (1976) and have been observed in many areas of the central nervous system. In birds, pruning of dendritic spines has been described in various animal model systems such as filial and sexual imprinting (Bischof, 1997;Bock and Braun, 1999;Bischof, 1996, 1998;Scheich et al, 1991;Wallhä usser and Scheich, 1987).…”

The Impact of Parent-Infant Interaction on Epigenetic Plasticity Mediating Synaptic Adaptations in the Infant Brain

“…This synaptic reorganization is the result of specific synaptic selection [47,48,49], which involves not only synaptic proliferation but also synaptic pruning (the removal of synaptic connections). Interestingly, the reduction of synaptic connections is accompanied by elevated metabolic activation upon presentation of the imprinting stimulus [47,48,50,51,52], which indicates that selective synaptic pruning increases the activity of this PFC analog. Moreover, using this animal model, it was shown for the first time that pruning of dendritic spine synapses requires neuronal activity, in particular glutamatergic, NMDA receptor-mediated synaptic activity, which is evoked by experience with the emotionally relevant imprinting object [48,53].…”