Distribution and intrinsic membrane properties of basal forebrain GABAergic and parvalbumin neurons in the mouse

The basal forebrain (BF) strongly regulates cortical activation, sleep homeostasis, and attention. Many BF neurons involved in these processes are GABAergic, including a subpopulation of projection neurons containing the calcium‐binding protein, parvalbumin (PV). However, technical difficulties in i...

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Published in:Journal of comparative neurology (1911) 2013-04, Vol.521 (6), p.1225-1250
Main Authors: McKenna, James T., Yang, Chun, Franciosi, Serena, Winston, Stuart, Abarr, Kathleen K., Rigby, Matthew S., Yanagawa, Yuchio, McCarley, Robert W., Brown, Ritchie E.
Format: Article
Language:English
Subjects:
Action potential
Animals
Brain
Cell Membrane - chemistry
Cell Membrane - metabolism
electrical coupling
GABAergic Neurons - chemistry
GABAergic Neurons - metabolism
Gene Knock-In Techniques
Glutamate Decarboxylase - analysis
Glutamate Decarboxylase - biosynthesis
glutamic acid decarboxylase
green fluorescent protein
H-current
Male
Mice
Neurons
parvalbumin
Parvalbumins - analysis
Parvalbumins - metabolism
Prosencephalon - chemistry
Prosencephalon - metabolism
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Summary:The basal forebrain (BF) strongly regulates cortical activation, sleep homeostasis, and attention. Many BF neurons involved in these processes are GABAergic, including a subpopulation of projection neurons containing the calcium‐binding protein, parvalbumin (PV). However, technical difficulties in identification have prevented a precise mapping of the distribution of GABAergic and GABA/PV+ neurons in the mouse or a determination of their intrinsic membrane properties. Here we used mice expressing fluorescent proteins in GABAergic (GAD67‐GFP knock‐in mice) or PV+ neurons (PV‐Tomato mice) to study these neurons. Immunohistochemical staining for GABA in GAD67‐GFP mice confirmed that GFP selectively labeled BF GABAergic neurons. GFP+ neurons and fibers were distributed throughout the BF, with the highest density in the magnocellular preoptic area (MCPO). Immunohistochemistry for PV indicated that the majority of PV+ neurons in the BF were large (>20 μm) or medium‐sized (15–20 μm) GFP+ neurons. Most medium and large‐sized BF GFP+ neurons, including those retrogradely labeled from the neocortex, were fast‐firing and spontaneously active in vitro. They exhibited prominent hyperpolarization‐activated inward currents and subthreshold “spikelets,” suggestive of electrical coupling. PV+ neurons recorded in PV‐Tomato mice had similar properties but had significantly narrower action potentials and a higher maximal firing frequency. Another population of smaller GFP+ neurons had properties similar to striatal projection neurons. The fast firing and electrical coupling of BF GABA/PV+ neurons, together with their projections to cortical interneurons and the thalamic reticular nucleus, suggest a strong and synchronous control of the neocortical fast rhythms typical of wakefulness and REM sleep. J. Comp. Neurol., 521:1225–1250, 2013. © 2012 Wiley Periodicals, Inc. The basal forebrain (BF) controls cortical activation, sleep homeostasis and attention. Many BF neurons involved in these processes are GABAergic, including a subpopulation of projection neurons containing the calcium binding protein, parvalbumin (PV). Here, we: (i) Validate novel genetic tools to investigate BF GABAergic and PV+ neurons; (ii) Provide the first comprehensive mapping of the distribution of GABAergic and PV+ neurons in the mouse; and (iii) Determine the intrinsic membrane properties of identified BF GABAergic and PV+ neurons. Figure legend: GFP selectively labels GABAergic neurons, but not cholinerg
ISSN:0021-9967
1096-9861
DOI:10.1002/cne.23290