Abstract
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.
Highlights
A wide range of studies in mammals have provided support for a model in which reward is signaled in the brain by increased activity of dopaminergic neurons in ventral tegmental area (VTA), and subsequent phasic dopamine release into forebrain areas [1,2,3]
In order to identify the type of neuron we recorded, dopaminergic and nondopaminergic neurons were distinguished after recordings by immunohistochemical staining for tyrosine hydroxylase (TH), or VTA projection neurons were identified during the experiment by the presence of a fluorescent tracer injected earlier into a target nucleus, Area X (Figure 1A)
We show that an affiliative social behavior can induce a similar synaptic plasticity in VTA dopaminergic neurons as pharmacological overactivation by addictive drugs [8,9,10]
Summary
A wide range of studies in mammals have provided support for a model in which reward is signaled in the brain by increased activity of dopaminergic neurons in VTA, and subsequent phasic dopamine release into forebrain areas [1,2,3]. Males produce a similar ‘undirected’ song when not in the presence of another bird These song types can be distinguished by subtle differences – the tempo of a male’s directed songs is typically slightly faster than that of his undirected songs, and details of fine acoustic structure are more variable from song to song during undirected singing [11,12,13]. When males sing to attract a female, but not when they sing while alone, the level of neural activity and the level of activity-dependent gene expression in a major dopaminergic input, VTA, is selectively modulated [19,20], and higher levels of dopamine can be measured in Area X [21] (Fig. 1) These studies support a model in which singing-related neural activity in the anterior forebrain pathway These studies support a model in which singing-related neural activity in the anterior forebrain pathway (Fig. 1; striatal Area X . dorsal lateral nucleus of the medial thalamus (DLM) -. pallial LMAN) is modulated by dopaminergic input from VTA during directed courtship singing, which reduces the variability of the output of the system to the motor pathway at RA, and biases song output to the higher stereotypy typical of courtship
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