Segregated anatomical input to sub-regions of the rodent superior colliculus associated with approach and defense.

The superior colliculus (SC) is responsible for sensorimotor transformations required to direct gaze toward or away from unexpected, biologically salient events. Significant changes in the external world are signaled to SC through primary multisensory afferents, spatially organized according to a retinotopic topography. For animals, where an unexpected event could indicate the presence of either predator or prey, early decisions to approach or avoid are particularly important. Rodents' ecology dictates predators are most often detected initially as movements in upper visual field (mapped in medial SC), while appetitive stimuli are normally found in lower visual field (mapped in lateral SC). Our purpose was to exploit this functional segregation to reveal neural sites that can bias or modulate initial approach or avoidance responses. Small injections of Fluoro-Gold were made into medial or lateral sub-regions of intermediate and deep layers of SC (SCm/SCl). A remarkable segregation of input to these two functionally defined areas was found. (i) There were structures that projected only to SCm (e.g., specific cortical areas, lateral geniculate and suprageniculate thalamic nuclei, ventromedial and premammillary hypothalamic nuclei, and several brainstem areas) or SCl (e.g., primary somatosensory cortex representing upper body parts and vibrissae and parvicellular reticular nucleus in the brainstem). (ii) Other structures projected to both SCm and SCl but from topographically segregated populations of neurons (e.g., zona incerta and substantia nigra pars reticulata). (iii) There were a few brainstem areas in which retrogradely labeled neurons were spatially overlapping (e.g., pedunculopontine nucleus and locus coeruleus). These results indicate significantly more structures across the rat neuraxis are in a position to modulate defense responses evoked from SCm, and that neural mechanisms modulating SC-mediated defense or appetitive behavior are almost entirely segregated.

Interactions between the Midbrain Superior Colliculus and the Basal Ganglia.

An important component of the architecture of cortico-basal ganglia connections is the parallel, re-entrant looped projections that originate and return to specific regions of the cerebral cortex. However, such loops are unlikely to have been the first evolutionary example of a closed-loop architecture involving the basal ganglia. A phylogenetically older, series of subcortical loops can be shown to link the basal ganglia with many brainstem sensorimotor structures. While the characteristics of individual components of potential subcortical re-entrant loops have been documented, the full extent to which they represent functionally segregated parallel projecting channels remains to be determined. However, for one midbrain structure, the superior colliculus (SC), anatomical evidence for closed-loop connectivity with the basal ganglia is robust, and can serve as an example against which the loop hypothesis can be evaluated for other subcortical structures. Examination of ascending projections from the SC to the thalamus suggests there may be multiple functionally segregated systems. The SC also provides afferent signals to the other principal input nuclei of the basal ganglia, the dopaminergic neurones in substantia nigra and to the subthalamic nucleus. Recent electrophysiological investigations show that the afferent signals originating in the SC carry important information concerning the onset of biologically significant events to each of the basal ganglia input nuclei. Such signals are widely regarded as crucial for the proposed functions of selection and reinforcement learning with which the basal ganglia have so often been associated.

A direct projection from superior colliculus to substantia nigra for detecting salient visual events.

Midbrain dopaminergic neurons respond to unexpected and biologically salient events, but little is known about the sensory systems underlying this response. Here we describe, in the rat, a direct projection from a primary visual structure, the midbrain superior colliculus (SC), to the substantia nigra pars compacta (SNc) where direct synaptic contacts are made with both dopaminergic and non-dopaminergic neurons. Complementary electrophysiological data reveal that short-latency visual responses in the SNc are abolished by ipsilateral lesions of the SC and increased by local collicular stimulation. These results show that the tectonigral projection is ideally located to relay short-latency visual information to dopamine-containing regions of the ventral midbrain. We conclude that it is within this afferent sensory circuitry that the critical perceptual discriminations that identify stimuli as both unpredicted and biologically salient are made.

Phasic activation of substantia nigra and the ventral tegmental area by chemical stimulation of the superior colliculus: an electrophysiological investigation in the rat.

The source of short-latency visual input to midbrain dopaminergic (DA) neurons is not currently known; however, the superior colliculus (SC) is a subcortical visual structure which has response latencies consistently shorter than those recorded for DA neurons in substantia nigra and the ventral tegmental area. To test whether the SC represents a plausible route by which visual information may gain short latency access to the ventral midbrain, the present study examined whether experimental stimulation of the SC can influence the activity of midbrain DA neurons. In urethane-anaesthetized rats, 63 pairs of extracellular recordings were obtained from neurons in the SC and ipsilateral ventral midbrain, before and after local disinhibitory injections of the GABA antagonist bicuculline (20-40 ng/200-400 nL saline) into the SC. Neurons recorded from substantia nigra and the ventral tegmental area were classified as putative DA (25/63, 39.7%) or putative non-DA (38/63, 60.3%). In nearly half the cases (27/63, 42.8%), chemical stimulation of the SC evoked a corresponding increase in neural activity in the ventral midbrain. This excitatory effect did not distinguish between DA and non-DA neurons. In 6/63 cases (9.5%), SC activation elicited a reliable suppression of activity, while the remaining 30/63 cases (47.6%) were unaffected. In almost a third of cases (16/57, 28.1%) intense phasic activation of the SC was associated with correlated phasic activation of neurons in substantia nigra and the ventral tegmental area. These data suggest that the SC is in a position to play an important role in discriminating the appropriate stimulus qualities required to activate DA cells at short latency.

Estudo das conexões aferentes do núcleo pré-mamilar dorsal (parte 1); caracterização da ativação do sistema nervoso central durante o comportamento predatório (parte 2)

O comportamento agressivo tem sido tradicionalmente categorizado em duas grandes classes, a saber: predatório e defensivo. Estudos recentes de nosso laboratório identificaram que um circuito distinto na zona medial do hipotálamo formado pelo núcleo hipotalâmico anterior, setor dorsomedial do núcleo ventromedial do hipotálamo e núcleo pré-mamilar dorsal (PMd), encontra-se particularmente ativo durante a expressão do comportamento de defesa frente a um predador. E experimentos revelam que o PMd parece ser uma peça chave neste circuito para a organização da resposta de defesa, uma vez que lesões bilaterais deste sítio hipotalâmico abolem esta resposta. Assim, na primeira etapa do presente trabalho fizemos um estudo sistemático dos sítios neurais que aferentam o PMd, usando inicialmente o método de rastreamento retrógrado de CTb, e confirmamos posteriormente as principais fontes de aferências com o uso de experimentos de rastreamento anterógrado com a técnica da leucoaglutinina de Phaseolus vulgaris. Nossos resultados revelam que o PMd recebe projeção de poucos sítios neurais a saber: núcleo hipotalâmico anterior, setores anterior e dorsomedial do núcleo ventromedial do hipotálamo, setor intermediolateral da área hipotalâmica lateral e núcleo tegmental ventral. Notamos que a projeção dos sítios hipotalâmicos para o PMd é bilateral, enquanto que aquela oriunda do núcleo tegmental ventral é unilateral. Se considerarmos as informações límbicas telencefálicas integradas ao nível das aferências do PMd, notamos que dentro do circuito da zona medial do hipotálamo mobilizado durante o comportamento de defesa, temos que o máximo de convergência de informações da esfera límbica prosencefálica ocorre ao nível do PMd. Por outro lado, informações oriundas do núcleo tegmental ventral podem veicular pistas espaciais de navegação do animal no ambiente. Na segunda etapa deste trabalho, caracterizamos os sistemas neurais mobilizados durante a execução do comportamento predatório, através da detecção imunohistoquímica da proteína Fos...(AU)