Afferent and efferent connections of the caudolateral neostriatum in the pigeon (Columba livia): A retro- and anterograde pathway tracing study

Abstract

The avian caudolateral neostriatum (NCL) was first identified on the basis of its dense dopaminergic innervation. This fact and data from lesion studies have led to the notion that NCL might be the avian equivalent of prefrontal cortex (PFC). A key feature of the PFC is the ability to integrate information from all modalities needed for the generation of motor plans. By using antero-and retrograde pathway tracing techniques, we investigated the organization of sensory afferents to the NCL and the connections with limbic and somatomotor centers in the basal ganglia and archistriatum. Data from all tracing experiments were compared with the distribution of tyrosine-hydroxylase (TH)-immunoreactive fibers, serving as a marker of dopaminergic innervation. The results show that NCL is reciprocally connected with the secondary sensory areas of all modalities and with at least two parasensory areas. Retrograde tracing also demonstrated further afferents from the deep layers of the Wulst and from the frontolateral neostriatum as well as the sources of thalamic input. Efferents of NCL project onto parts of the avian basal ganglia considered to serve somatomotor or limbic functions. Projections to the archistriatum are mainly directed to the somatomotor part of the intermediate archistriatum. In addition, cells in caudal NCL were found to be connected with the ventral and posterior archistriatum, which are considered avian equivalents of mammalian amygdala. All afferents and projection neurons were confined to the plexus of densest TH innervation. Our results show that the NCL is positioned to amalgamate information from all modalities and to exert control over limbic and somatomotor areas. This organization might comprise the neural basis for such complex behaviours as working memory or spatial orientation.

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

“…Because we find a similar representation of novel and familiar stimuli with the same behavioral meaning, the NCL might be a source of an abstract task-relevant signal that biases representations in higher sensory areas to encode behaviorally meaningful stimuli, similar to the top-down signal from the PFC to the temporal cortex (19). Like the PFC, the NCL has reciprocal connectivity to all sensory association areas, putting it in a prime position for such executive control over sensory processing and behavior (6,26).…”

Revised nomenclature for avian telencephalon and some related brainstem nuclei

“…This region was called the dorsal archistriatum in Karten and Hodos (1967), but in their reformulation of the archistriatum, Zeier and Karten (1971) renamed this region the dorsal part of the intermediate archistriatum. By neurochemistry and connections, it is a distinct region (Wä chtler, 1985;Wä chtler and Ebinger, 1989;Medina and Reiner, 1994;Reiner et al, 1994;Veenman et al, 1995b;Kröner and Gü ntü rkü n, 1999;Sun and Reiner, 2000). The Forum recommended this region be renamed the dorsal arcopallium (Table 5,Figs.…”

“…This region constituted the dorsal part of the ventral archistriatum in Karten and Hodos (1967), but in their reformulation of the archistriatum, Zeier and Karten (1967) renamed this region the intermediate archistriatum. By neurochemistry and connections, it is distinct from what has until now been called the dorsal intermediate archistriatum (Wä chtler, 1985;Wä chtler and Ebinger, 1989;Reiner et al, 1994;Veenman et al, 1995b;Kröner and Gü ntü rkü n, 1999;Sun and Reiner, 2000). The Forum recommended that the intermediate archistriatum be renamed the intermediate arcopallium, with "pars ventralis" not needed due to the deletion of "intermediate" from the name for the dorsal arcopallium (Table 5,Figs.…”

Out of Context: NMDA Receptor Antagonism in the Avian 'Prefrontal Cortex' Impairs Context Processing in a Conditional Discrimination Task.

“…Against this background, it seems to be premature to speculate about equivalencies of subfields of the NCL and the PFC, although there is some evidence for a parcellation of the NCL Kröner & Güntürkün, 1999;Riters, Erichsen, Krebs, & Bingman, 1999). We therefore have refrained from comparing the NCL with specific PFC subfields and instead have discussed the contextprocessing function of the NCL as a whole.…”

“…This conclusion rests on a large data set involving neuroanatomical, physiological, neurochemical, and behavioral results. Neuroanatomical studies showed the NCL to receive multimodal input from all secondary sensory areas of the forebrain (Leutgeb, Husband, Riters, Shimizu, & Bingman, 1996), to project to telencephalic motor output structures as well as to the basal ganglia (Kröner and Güntürkün, 1999), to be innervated by dopaminergic fibers from midbrain cell groups A8 -A10 (Metzger, Jiang, Wang, & Braun, 1996), and to be characterized by a high density of dopamine D 1 receptors (Schnabel et al, 1997). Physiological studies demonstrated that single units in the NCL code for the upcoming reward (Kalt, Diekamp, & Güntürkün, 1999), bridge the delay between stimulus and response by high sustained activity levels (Diekamp, Kalt, & Güntürkün, 2002), and code for the subjective reward value of a reinforcer (Kalenscher et al, 2005).…”