Common Features of Neural Activity during Singing and Sleep Periods in a Basal Ganglia Nucleus Critical for Vocal Learning in a Juvenile Songbird

Reactivations of waking experiences during sleep have been considered fundamental neural processes for memory consolidation. In songbirds, evidence suggests the importance of sleep-related neuronal activity in song system motor pathway nuclei for both juvenile vocal learning and maintenance of adult song. Like those in singing motor nuclei, neurons in the basal ganglia nucleus Area X, part of the basal ganglia-thalamocortical circuit essential for vocal plasticity, exhibit singing-related activity. It is unclear, however, whether Area X neurons show any distinctive spiking activity during sleep similar to that during singing. Here we demonstrate that, during sleep, Area X pallidal neurons exhibit phasic spiking activity, which shares some firing properties with activity during singing. Shorter interspike intervals that almost exclusively occurred during singing in awake periods were also observed during sleep. The level of firing variability was consistently higher during singing and sleep than during awake non-singing states. Moreover, deceleration of firing rate, which is considered to be an important firing property for transmitting signals from Area X to the thalamic nucleus DLM, was observed mainly during sleep as well as during singing. These results suggest that songbird basal ganglia circuitry may be involved in the off-line processing potentially critical for vocal learning during sensorimotor learning phase

Social Modulation during Songbird Courtship Potentiates Midbrain Dopaminergic Neurons

Synaptic transmission onto dopaminergic neurons of the mammalian ventral tegmental area (VTA) can be potentiated by acute or chronic exposure to addictive drugs. Because rewarding behavior, such as social affiliation, can activate the same neural circuitry as addictive drugs, we tested whether the intense social interaction of songbird courtship may also potentiate VTA synaptic function. We recorded glutamatergic synaptic currents from VTA of male zebra finches who had experienced distinct social and behavioral conditions during the previous hour. The level of synaptic transmission to VTA neurons, as assayed by the ratio of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) to N-methyl-D-aspartic acid (NMDA) glutamate receptor mediated synaptic currents, was increased after males sang to females, and also after they saw females without singing, but not after they sang while alone. Potentiation after female exposure alone did not appear to result from stress, as it was not blocked by inhibition of glucocorticoid receptors. This potentiation was restricted to synapses of dopaminergic projection neurons, and appeared to be expressed postsynaptically. This study supports a model in which VTA dopaminergic neurons are more strongly activated during singing used for courtship than during non-courtship singing, and thus can provide social context-dependent modulation to forebrain areas. More generally, these results demonstrate that an intense social encounter can trigger the same pathways of neuronal plasticity as addictive drugs

Behavioural and neural lateralisation of vision in courtship singing of the zebra finch

International audienceLateralised function has been observed in a number of animal species. Most studies on the lateralisation of visually guided behaviour indicate a preferential use of the right eye/left hemisphere in food discrimination in chicks, pigeons and zebra finches. One study reported a right eye/left hemisphere dominance in courtship behaviour of male zebra finches, but this result was later disputed. Here we provide clear evidence of lateralised visual function in zebra finch courtship singing, and initial evidence for neural lateralisation. Behavioural experiments using the temporary occlusion of one eye showed that, when presented with a female, male birds tended to start singing later and sang significantly less in both monocular conditions than in binocular condition. Most importantly, birds sang 1.2 times more when using their right than left eye, and they especially sang significantly more motifs. At the central level, the evaluation of the density of ZENK- or Fos-positive cells in the optic tectum showed that the expression of these immediate early genes was significantly higher in several layers of the left than the right optic tectum. The fact that birds sang significantly more motifs when using their right than left eye suggests that there is a preference for visual processing by the right eye during courtship singing. A functional predominance of the left hemisphere processing is further supported by the significantly higher level of expression of immediate early genes in the left optic tectum. Both of these results are consistent with the proposed specialization of the avian left hemisphere in sustaining attention on stimuli, in this context the female zebra finch, to which a motor response is planned. In the future, simultaneous recordings of neuronal activity from both hemispheres will allow us to further characterize such hemispheric specialization

Behavioral and neural lateralization of vision in courtship singing of the zebra finch

WOS:000239905800011International audienceAlong with human speech and language processing, birdsong has been one of the best-characterized model systems for understanding the relationship of lateralization of brain function to behavior. Lateralization of song production has been extensively characterized, and lateralization of song perception has begun to be studied. Here we have begun to examine whether behavior and brain function are lateralized in relation to communicative aspects of singing, as well. In order to monitor central brain function, we assayed the levels of several activity dependent immediate early genes after directed courtship singing. Consistent with a lateralization of visual processing during communication, there were higher levels of expression of both egr-1 and c-fos in the left optic tectum after directed singing. Because input from the eyes to the brain is almost completely contralateral in birds, these results suggest that visual input from the right eye should be favored during normal singing to females. Consistent with this, we further found that males sang more when they could use only their right eye compared to when they could use only their left eye. Normal levels of singing, though, required free use of both eyes to view the female. These results suggest that there is a preference for visual processing by the right eye and left brain hemisphere during courtship singing. This may reflect a proposed specialization of the avian left hemisphere in sustaining attention on stimuli toward which a motor response is planned. (c) 2006 Wiley Periodicals, Inc

Behavioural and neural lateralisation of vision in courtship singing of the zebra finch

International audienceLateralised function has been observed in a number of animal species. Most studies on the lateralisation of visually guided behaviour indicate a preferential use of the right eye/left hemisphere in food discrimination in chicks, pigeons and zebra finches. One study reported a right eye/left hemisphere dominance in courtship behaviour of male zebra finches, but this result was later disputed. Here we provide clear evidence of lateralised visual function in zebra finch courtship singing, and initial evidence for neural lateralisation. Behavioural experiments using the temporary occlusion of one eye showed that, when presented with a female, male birds tended to start singing later and sang significantly less in both monocular conditions than in binocular condition. Most importantly, birds sang 1.2 times more when using their right than left eye, and they especially sang significantly more motifs. At the central level, the evaluation of the density of ZENK- or Fos-positive cells in the optic tectum showed that the expression of these immediate early genes was significantly higher in several layers of the left than the right optic tectum. The fact that birds sang significantly more motifs when using their right than left eye suggests that there is a preference for visual processing by the right eye during courtship singing. A functional predominance of the left hemisphere processing is further supported by the significantly higher level of expression of immediate early genes in the left optic tectum. Both of these results are consistent with the proposed specialization of the avian left hemisphere in sustaining attention on stimuli, in this context the female zebra finch, to which a motor response is planned. In the future, simultaneous recordings of neuronal activity from both hemispheres will allow us to further characterize such hemispheric specialization

Social behavior modulates songbird interpeduncular nucleus function

International audienceMale zebra finches produce the same song while alone and during courtship of a female. However, singing-related activity in the anterior forebrain nuclei lateral magnocellular anterior nidopallium and Area X markedly depends on the social context. Thus, the anterior forebrain should receive a signal of social context from outside the song system. Here we investigated a possible source of such modulation, the midbrain interpeduncular nucleus, by monitoring immediate early genes and synaptic activity. The level of immunoreactivity for egr1 was high and calretinin was low following courtship directed singing, but the opposite pattern was seen after solo undirected singing. Further, pairs of stimulation caused depression of synaptic responses after directed singing, but facilitation after undirected singing