Intrinsic and synaptic properties of neurons in the vocal-control nucleus lMAN fromin vitro slice preparations of juvenile and adult zebra finches

Abstract

A common theme of diverse neural systems is that circuits that are important for initial acquisition of learning do not necessarily serve as a substrate for the long‐term storage of that memory. The neural basis of vocal learning in songbirds provides an example of this phenomenon, since a circuit that is necessary for vocal production during initial stages of vocal development apparently plays no subsequent role in controlling learned vocalizations. This striking functional change suggests the possibility of marked physiological changes in synaptic transmission within this circuit. We therefore examined intrinsic and synaptic properties of neurons in the cortical nucleus lMAN (lateral magnocellular nucleus of the anterior neostriatum), which forms part of this developmentally regulated circuit, in an in vitro preparation of the zebra finch forebrain. Although both functional and morphological characteristics of these neurons change substantially during vocal development, we did not observe widespread, substantive changes in the electrophysiological characteristics of juvenile versus adult lMAN neurons examined in vitro. Overall, both the intrinsic properties and synaptic responses of lMAN neurons were similar in slices from juvenile birds (at ages when lesions of lMAN disrupt vocal production) and in slices from adult birds (when lMAN lesions have no effect on song production). However, one intrinsic property that did vary between juvenile and adult cells was spike duration, which was longer in juvenile cells, suggesting the potential for activation of second‐messenger cascades and/or enhanced synaptic transmission onto target cells of lMAN neurons. The pattern of synaptic response observed in both juvenile and adult cells suggests that lMAN projection neurons receive direct excitatory afferent inputs, as well as disynaptic inhibitory inputs from interneurons within lMAN. Activation of inhibitory interneurons rapidly curtails the excitatory response seen in projection neurons. This inhibition was abolished by bicuculline, indicating that the inhibitory interneurons normally exert their postsynaptic response via GABAA receptors on projection neurons. The inhibitory response could also be blocked by CNQX (6‐cyano‐7‐nitroquinoxaline‐2,3‐dione), suggesting that the activation of inhibitory interneurons within lMAN may be governed primarily by AMPA receptors. © 1998 John Wiley & Sons, Inc. J Neurobiol 37: 642–658, 1998

Genomics analysis of potassium channel genes in songbirds reveals molecular specializations of brain circuits for the maintenance and production of learned vocalizations

“…LMAN’s core region contains magnocellular neurons that send dual projections to Area X and RA, as well as GABAergic neurons that influence the projection neurons through inhibition [62,63]. The magnocellular neurons are of particular interest since they provide direct input to the AFP via Area X, and the DMP via RA.…”

Expression of the GABAA receptor γ4-subunit gene in discrete nuclei within the zebra finch song system

“…Consistent with this, the presence of functional GABA type A (GABA A ) receptors, within the song system, has been 6 demonstrated electrophysiologically by a number of groups (Livingston and Mooney, 1997;Bottjer et al, 1998;Luo and Perkel, 1999;Vicario and Raksin, 2000;Pinaud et al, 2004;Farries et al, 2005;Mooney and Prather, 2005), although a detailed pharmacological characterisation is lacking. For example, picrotoxin and bicuculline block receptors on neurons within the LMAN (Livingston and Mooney, 1997;Bottjer et al, 1998), the DLM (Luo and Perkel, 1999), the HVC (Mooney and Prather, 2005), the RA (Vicario and Raksin, 2000) and Area X (Farries et al, 2005). From this body of work, it appears that GABA A receptors, which are a family of post-synaptic proteins, play an important role in the learning and production of song in the zebra finch.…”

“…A significant body of literature has strongly implicated GABA A receptors in the regulation of excitation within the zebra finch song system (Livingston and Mooney, 1997;Bottjer et al, 1998;Luo and Perkel, 1999;Cardin and Schmidt, 2004;Pinaud et al, 2004;Farries et al, 2005;Mooney and Prather, 2005). These receptors are the major inhibitory neurotransmitter receptors in brain, and they exist in a variety of forms called subtypes, that are assembled from seven different types of subunit (, , , , ,  and ; Darlison et al, 2005;Sieghart, 2006).…”

“…And, recently, the distribution of GABAergic cells within the zebra finch telencephalon has been mapped, using a glutamic acid decarboxylase riboprobe (Pinaud et al, 2004) and an anti-GABA antibody (Pinaud and Mello, 2007). Consistent with this, the presence of functional GABA type A (GABA A ) receptors, within the song system, has been 6 demonstrated electrophysiologically by a number of groups (Livingston and Mooney, 1997;Bottjer et al, 1998;Luo and Perkel, 1999;Vicario and Raksin, 2000;Pinaud et al, 2004;Farries et al, 2005;Mooney and Prather, 2005), although a detailed pharmacological characterisation is lacking. For example, picrotoxin and bicuculline block receptors on neurons within the LMAN (Livingston and Mooney, 1997;Bottjer et al, 1998), the DLM (Luo and Perkel, 1999), the HVC (Mooney and Prather, 2005), the RA (Vicario and Raksin, 2000) and Area X (Farries et al, 2005).…”

Dynamic top-down biasing implements rapid adaptive changes to individual movements

“…Prior literature suggests that a substantial portion of the spikes we recorded was from excitatory projection neurons. First, for LMAN, the ratio of projection neurons to interneurons has been estimated at around 3:1 ( Bottjer et al, 1998 ) to 15:1 ( Livingston and Mooney, 1997 ). Further evidence that excitatory neurons are more easily detected than inhibitory ones comes from reports of difficulty finding interneurons in slice preparations ( Boettiger and Doupe, 1998 ; Livingston and Mooney, 1997 ).…”