The dorsocaudal neostriatum of the domestic chick: a structure serving higher associative functions

Abstract

The dorsocaudal neostriatal (dNC) complex consists of at least three functionally distinct subregions and is part of an `imprinting' pathway, which interconnects several forebrain regions that are known to be involved in juvenile learning. Based on its anatomical features, at least one subregion of the dNC complex, the neostriatum dorsocaudale (Ndc) may be considered as the equivalent of the mammalian polysensory association cortices. Several lines of evidence point to a role for this forebrain region in learning and memory formation. After auditory or visual imprinting changes of stimulus-evoked metabolic activities and of synaptic densities have been measured in the Ndc. Pharmacological behavioral studies revealed that the activation of NMDA receptors plays a critical role during this learning process and that NMDA receptor activation is required for the associated metabolic and synaptic changes. In addition to glutamatergic afferents, anatomical studies revealed a massive input from monoaminergic and peptidergic pathways into the dNC complex, suggesting a modulatory role for these systems during imprinting. The results presented here together with data from other avian species support the view that the dNc complex, and in particular the Ndc, plays an important role in juvenile and adult learning.

Introduction

The process of rapid development of social attachments, which is classically termed filial `imprinting', can be characterized by the restriction to sensitive phases of life, the velocity and the stability of the acquired information and behavioral strategies 1, 4, 20, 48. Filial imprinting, i.e. the formation of an emotional attachment between the newborn and the parents, particularly the mother, has been described in a variety of vertebrate species including birds, rodents, primates and man 9, 16, 18, 21, 34, 40, 50. Studies in primates and humans have shown clearly that the amount of social experience during early childhood and the intensity of the emotional relationship to the caregiver is of great importance for the normal development of intellectual and emotional maturity and communication skills 19, 47, 49.

In particular, because of this exceptionally long-lasting impact of juvenile emotional experience and learning events, visual or acoustic filial imprinting in precocial birds provides an attractive experimental model for the systematic analysis of synaptic plasticity. Since the juvenile brain is assumed to be equipped with mechanisms of synaptic plasticity auxiliary to those found in the adult brain, learning-induced synaptic changes may be more pronounced and occur more rapidly. It is tempting to speculate that the stability of imprinted information and behavioral strategies is due to a long-lasting or even permanent reorganization of synaptic connections, which is elicited and modulated by early postnatal learning 40, 41. This reorganization of synaptic connections and functional brain circuits may lead to the formation of an efficient synaptic matrix, which lays the foundation for later learning in adulthood.

Under laboratory conditions, newly hatched chicks imprint easily on a mother surrogate, on rhythmic tone-pulses 3, 25, 40, 52, or on visual stimuli of different shapes and/or colors 1, 4, 20, 50. Several forebrain areas have been identified, in which the presentation of a learned acoustic or visual stimulus evokes an enhanced metabolic and electric activation. Some regions, such as the intermediate and medial hyperstriatum ventrale (IMHV) are preferentially activated by visual stimuli 6, 11, 20, 33and therefore seem to be predominantly involved in the processing of visual imprinting stimuli. The medio-rostral neostriatum/hyperstriatum (MNH) shows a pronounced activation during acoustic stimulation and hence appears to be mainly dedicated to the processing of acoustic imprinting stimuli 3, 10, 25, 52. However, natural imprinting objects usually consist of a combination of visual and acoustic components. Thus, besides such specialized associative forebrain regions, the existence of one or several higher associative brain regions must be postulated as polymodal associative parts of the `imprinting' pathway (see below), in which different sensory and emotional components are integrated during the learning process, and also during memory recall. This polymodal association area may be relayed to the MNH and IMHV, respectively, and thereby provide indirect sensory information to these regions (Fig. 1). One candidate for such an integrative polymodal associative forebrain region is a subregion in the dorsocaudal neostriatal (dNC) complex, an area termed the neostriatum dorsocaudale (Ndc) 2, 29, 30, 41.