Prosencephalic pathways related to the paleostriatum of the pigeon (Columba livia)

doi:10.1016/0006-8993(78)90836-3

Brain Research

Volume 147, Issue 2, 26 May 1978, Pages 205-221

https://doi.org/10.1016/0006-8993(78)90836-3 Get rights and content

Abstract

Afferent connections of the avian paleostriatal complex were traced by means of anterograde and retrograde transport of horseradish peroxidase (HRP). The paleostriatum augmentatum (PA), a cell field comparable to mammalian caudate nucleus and putamen, was found to receive projections from a distinct population of telencephalic neurons in the temporal-parietal-occipital (TPO) and lateral cortical (CDL) areas of the neostriatum. TPO neurons, in turn, were found to receive projections from the contralateral ventral archistriatum (Av) and from neurons in the ipsilateral frontal neostriatum adjacent to the rostal portion of the ectostriatum (E). The paleostriatum primitivum (PP), comparable to globus pallidus, receives projections from the small cells of PA, and from neurons in the anterior nucleus of the ansa lenticularis (ALa). ALa appears similar to the mammalian subthalamic nucleus of the basis of its afferent and efferent connections. In addition, PA was also found to receive extensive projections from the nucleus tegmenti pedunculopontinus of the midbrain, a dopamine-containing cell group. Evidence of projections from the nucleus dorsointermedius posterior (DIP), a cell group receiving both cerebellar and paleostriatal afferents, to the rostral telencephalon was also found.

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The avian striatum, like the mammalian striatum, develops from a Dlx1/2-rich and Nkx2.1-poor neuroepithelium (Fernandez et al., 1998; Puelles et al., 2000). The mammalian striatum contains neurochemically and hodologically distinct striosomes (or patches) dispersed within the striatal matrix, but such a segregation of patches within the striatal matrix is not obvious in birds (Karten and Dubbeldam, 1973; Brauth et al., 1978; Reiner et al., 1983, 1994, 1998a; Bottjer et al., 1989; Bottjer, 1993; Castro and Ball, 1994; Grisham and Arnold, 1994; Medina and Reiner, 1995; Soha et al., 1996; Durstewitz et al., 1999; Luo and Perkel, 1999). The matrix compartment of mammalian striatum is further divided into functional territories (termed T1-T3 by Morel et al., 2002) that are distinguished by their neuropil content of different markers, in particular CALB and PARV (Morel et al., 2002; François et al., 1994; Holt et al., 1997; Joel and Weiner, 1997; Prensa et al., 2003; Riedel et al., 2002).
The goals of this study were to use multiple informative markers to define and characterize the neurochemically distinct compartments of the pigeon basal ganglia, especially striatum and accumbens. To this end, we used antibodies against 12 different neuropeptides, calcium-binding proteins or neurotransmitter-related enzymes that are enriched in the basal ganglia. Our results clarify boundaries between previously described basal ganglia subdivisions in birds, and reveal considerable novel heterogeneity within these previously described subdivisions. Sixteen regions were identified that each displayed a unique neurochemical organization. Four compartments were identified within the dorsal striatal region. The neurochemical characteristics support previous comparisons to part of the central extended amygdala, somatomotor striatum, and associational striatum of mammals, respectively. The medialmost part of the medial striatum, however, has several unique features, including prominent pallidal-like woolly fibers and thus may be a region unique to birds. Four neurochemically distinct regions were identified within the pigeon ventral striatum: the accumbens, paratubercular striatum, ventrocaudal striatum, and the ventral area of the lateral part of the medial striatum that is located adjacent to these regions. The pigeon accumbens is neurochemically similar to the mammalian rostral accumbens. The pigeon paratubercular and ventrocaudal striatal regions are similar to the mammalian accumbens shell. The ventral portions of the medial and lateral parts of the medial striatum, which are located adjacent to accumbens shell-like areas, have neurochemical characteristics as well as previously reported limbic connections that are comparable to the accumbens core. Comparisons to neurochemically identified compartments in reptiles, mammals, and amphibians indicate that, although most of the basic compartments of the basal ganglia were highly conserved during tetrapod evolution, uniquely avian compartments may exist as well.
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Citation Excerpt :
The pallium in birds contains the same subdivisions as in reptiles but is considerably expanded, with its dorsal part enlarged into a medially situated sensorimotor region called the Wulst (comparable to reptile dorsal cortex) and the DVR (consisting of the mesopallium and nidopallium) juxtaposed to a basocaudal motor output area called the arcopallium. The Wulst, DVR, and arcopallium give rise to a massive excitatory input to the avian striatum (Brauth et al., 1978; Davies et al., 1997; Dubbeldam and Visser, 1987; Dubbeldam et al., 1997; Karten and Dubbeldam, 1973; Karten et al., 1973; Nottebohm et al., 1976; Veenman and Reiner, 1996; Veenman et al., 1995b; Wild, 1987b, 1989; Wild et al., 1993; Zeier and Karten, 1971). As in mammals, the avian “corticostriatal” projection largely ends on the heads of the dendritic spines of striatal projection neurons and utilizes the excitatory neurotransmitter glutamate (Adam and Csillag, 2006; Csillag et al., 1997; Laverghetta et al., 2006; Veenman and Reiner, 1996).
A striatum and pallidum have been basal ganglia constituents since early in vertebrate evolution, underlining what is now known about their functional interrelatedness. The most noteworthy evolutionary change in the basal ganglia appears to have accompanied the overall telencephalic enlargement and elaboration of thalamic sensory inputs to the pallium that occurred at the anamniote–amniote transition. At this transition, basal ganglia size and cell abundance increased, and afferent and efferent circuits linking it to the pallium became prominent. Nonetheless, the role of the basal ganglia in motor control appears ancient, and in nonmammals is mediated mainly via the midbrain.
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The forebrain of birds comprises the pallium or cortical-like region that surrounds a heterogeneous core called the subpallium. The purpose of this review is to define the structural components of the subpallium utilizing a revised nomenclature for the avian forebrain and provide proposed functions for this brain region. The subpallium includes five major groups including the dorsal somatomotor basal ganglia, ventral viscerolimbic basal ganglia, extended amygdala, basal telencephalic cholinergic and non-cholinergic corticopetal system, and septum and septal neuroendocrine systems. Proposed functions for each of the five groups are discussed and where appropriate each structural and functional group is compared to that in mammals. Importantly, structures within the subpallium are known to project to components of the autonomic nervous system (ANS), which are briefly described. A major group of gonadotropin-releasing hormone neurons resides within the fifth principal group, the septum, and therefore the neuroendocrine role of the subpallium, particularly in affecting anterior pituitary function related to the reproductive system, is reviewed. A second key function associated with the ANS and subpallium is the regulation of food intake and energy balance. In birds, particularly migratory species, there appears to be shifts in set points of body weight due to seasonal metabolic needs of various avian species. An autonomic hypothesis, termed poikilostasis, based upon shifts in homeostatic set points of body weight regulation is presented that may be relevant in explaining the large changes in seasonal body weight and body composition in migratory birds throughout their annual cycle. Similarly, the clear changes in body weight and composition of broilers and broiler breeders due to their selection for growth rate and feed conversion may also be related to a shift in the balance of the two antagonistic arms of the ANS.
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Citation Excerpt :
As in mammals, the “corticostriatal” projection utilizes glutamate, an excitatory amino acid neurotransmitter (Csillag et al., 1997; Ding and Perkel, 2004; Ding et al., 2003; Farries et al., 2005a; Reiner et al., 2001; Veenman and Reiner, 1996). More lateral MSt receives pallial input from somatic regions, such as those involved in somatosensory, visual, auditory and motor function (Brauth et al., 1978; Karten and Dubbeldam, 1973; Nottebohm et al., 1976; Veenman et al., 1995; Wild, 1987; Wild et al., 1993). By contrast, medial MSt appears more viscerolimbic, since its pallial input arises from such regions as hippocampus and olfactory bulb.
The subpallial region of the avian telencephalon contains neural systems whose functions are critical to the survival of individual vertebrates and their species. The subpallial neural structures can be grouped into five major functional systems, namely the dorsal somatomotor basal ganglia; ventral viscerolimbic basal ganglia; subpallial extended amygdala including the central and medial extended amygdala and bed nuclei of the stria terminalis; basal telencephalic cholinergic and non-cholinergic corticopetal systems; and septum. The paper provides an overview of the major developmental, neuroanatomical and functional characteristics of the first four of these neural systems, all of which belong to the lateral telencephalic wall. The review particularly focuses on new findings that have emerged since the identity, extent and terminology for the regions were considered by the Avian Brain Nomenclature Forum. New terminology is introduced as appropriate based on the new findings. The paper also addresses regional similarities and differences between birds and mammals, and notes areas where gaps in knowledge occur for birds.

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Prosencephalic pathways related to the paleostriatum of the pigeon (Columba livia)

Abstract

Brain Research

Brain Research

Brain Research

The comparative Anatomy of the Neurons System of Vertebrates, Including Man

Organization of the tectofugal visual pathway in the pigeon: a retrograde transport study

J. comp. Neurol.

Relations between the optic tectum and basal ganglia in the pigeon

Neurosci. Abstr.

Efferent fibers of the subthalamic nucleus in the monkey: A comparison of the efferent projections of the subthalamic nucleus, substantia nigra and globus pallidus

Amer. J. Anat.

The radial fibers in the globus pallidus

J. comp. Neurol.

An intricately patterned prefrontocaudate projection in the rhesus monkey

J. comp. Neurol.

3rigin and distribution of nigro-tectal fibers in the cat

Neurosci. Abstr.