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Neuronal Activity Within the Nucleus Basalis and Conditioned Neocortical Electroencephalographic Activation

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The Journal of Neuroscience, March 1994, 74(3): 1623-i 633 Neuronal Activity within the Nucleus Basalis and Conditioned Neocortical Electroencephalographic Activation Paul J. Whalen, Bruce S. Kapp, and Jeffrey P. Pascoe Department of Psychology, The University of Vermont, Burlington, Vermont 05405 The relationship between neuronal activity within the nucle- behavioral arousal, and synchronization, or the enhanced in- us basalis (NB) and conditioned neocortical EEG activation cidence of high-amplitude slow activity, reflective of decreased was investigated in New Zealand rabbits during Pavlovian arousal (Jasperand Carmichael, 1935; Rheinberger and Jasper, differential conditioning. Twenty-seven of 56 neurons re- 1937). corded in conditioned animals demonstrated a significantly Recent researchhas demonstrated that stimulation of the NB greater change in activity to a tone (CS+) that predicted the produces EEG desynchronization (Berladetti et al., 1977; Cas- occurrence of a mildly aversive unconditioned stimulus when amenti et al., 1986; Metherate et al., 1992) and increasesin the compared to a tone (CS-) that did not. Twenty-four of these extracellular concentration of ACh in the neocortex (Casamenti 27 neurons demonstrated a significant increase in activity et al., 1986). Furthermore, lesions of the NB that deplete the to the CS+ compared to the CS-, while the remaining three neocortex of ACh produce an increasein high-amplitude slow neurons demonstrated a significant decrease in activity to activity (e.g., 6 activity) in the EEG (Stewart et al., 1984; Buzsaki the CS+ compared to the CS-. In 24 of these 27 neurons et al., 1988; P. Riekkinen Jr. et al., 1990) similar to that observed (69%) these changes in neuronal activity during CS presen- after administration of cholinergic antagonists (Longo, 1966; tations correlated significantly with a decrease in the power Buzsaki et al., 1988; Metherate et al., 1992). A contribution for of 6 activity in the EEG. In addition, 13 of these 24 neurons the NB in neocortical activation receives additional support (54%) demonstrated significant correlations between neu- from the findings that (1) stimulation of the NB facilitates the ronal activity and the power of 6 activity during CS-free pe- responsivenessof sensoryneocortical neuronsto sensorystimuli riods. In experimentally naive animals, the activity of 10 of (Metherate and Ashe, 1991) (2) lesions of the NB reduce the 22 neurons (45%) recorded within the region of the NB cor- responsivenessof neurons in the visual cortex to visual stimuli related with the power of 6 activity in the EEG during stim- (Sato et al., 1987) and (3) ACh, when applied to neocortical ulus-free periods. These results complement a growing body sensory neurons, produces a striking enhancementof their re- of evidence and provide strong support for the hypothesis sponseto sensory stimuli (Sillito and Kemp, 1983; Metherate that the NB contributes to neocortical activation in the con- et al., 1987, 1988). scious animal. These combined observations are consistent with the notion [Key words: electroencephalography, nucleus basalis, that cholinergic neurons of the NB function to activate the neo- substantia innominata, rabbit, Pavlovian conditioning, arous- cortex, providing a cortical state that reflects an enhancedreadi- al, 6 activity] nessof neurons to respond to afferent input and perhaps pro- viding a cellular substrate for an enhanced state of behavioral The nucleus basalis of Meynert (NB) is a diffuse grouping of alertnessor arousal. Such a function would dictate that neurons neurons within the basal forebrain that projects to widespread within the NB region should respond to stimuli that elicit be- areas of the neocortex and that representsthe main source of havioral and neocortical arousal, as reflected in EEG desyn- neocortical ACh (Divac, 1975; Mesulam and Van Hoesen, 1976; chronization. Indeed, neurons within the NB region demon- Johnston et al., 1979; Lehmann et al., 1980; Wenk et al., 1980; strate altered rates of activity in responseto stimuli predictive Mesulam et al., 1983a,b; Saper, 1984; Russchenet al., 1985). of reward (Rigdon and Pirch, 1986; Richardson and Delong, Given the long-term association of ACh with neocorticai acti- 1990; Wilson and Rolls, 1990), stimuli that presumably elicit vation or arousal (Wikler, 1952; Celesiaand Jasper, 1966; Lon- increasedlevels of behavioral arousal. Furthermore, Detari and go, 1966; Szerb, 1967) researchhas been directed toward the Vanderwolf (1987) have demonstrated in the urethane-anes- contributions of the NB to neocortical activation, as reflected thetized rat that neurons within the NB increase their activity in low-voltage fast activity or EEG desynchronization. This during periods of EEG desynchronization in responseto tail- EEG pattern has long been used as a quantitative, objective pinch. In addition, Buzsaki et al. (1988) observed that NB neu- measureof different levels of alertnessor behavioral arousal in rons in the rat fired at a higher rate during walking, when the the awake state, with desynchronization reflective of heightened EEG was characterized by desynchronization, than during im- mobility, when the EEG showeda higher incidence of 6 activity. Received June 1 I, 1993; accepted Aug. 26, 1993. However, a systematic, quantitative analysis of the extent to This study was supported by NSF Grant BNS 9010760 to B.S.K. We thank Dr. which the activity of these neurons correlates with the magni- William F. Supple for assistance with electrophysiological recording and Jason tude of EEG desynchronization in the consciousanimal in the Fechter for assistance with data analysis. Correspondence should be addressed to Paul J. Whalen at the above address. presenceof emotionally arousing stimuli that elicit EEG desyn- Copyright 0 1994 Society for Neuroscience 0270-6474/94/141623-l 1$05.00/O chronization has yet to be undertaken. The present study, there- 1624 Whalen et al. - Nucleus Basalis and EEG Activation fore, was designed to determine if (1) neurons within the NB placed within a shielded, ventilated, and sound-attenuating recording respond differentially to conditioned auditory stimuli that signal chamber (Industrial Acoustics Co.) that was equipped with a 24 cm either the presence or absence of a mildly aversive event and speaker situated 48 cm in front ofthe animal, and a modified stereotaxic frame used to immobilize the animal’s head. Responses of single neu- that therefore elicit differential levels of neocortical arousal as rons were amplified by a high-impedance, differential preamplifier (DAM- reflected in EEG desynchronization in the conscious rabbit, and 50, World Precision Instruments) coupled with a main amplifier (7P5 11, (2) the activity of these neurons in response to these stimuli Grass Instruments) and a custom-made active filter, for a total system significantly correlates with the magnitude of the EEG desyn- gain of approximately 25 k and a bandwidth of 0.3-10 kHz. Responses from single neurons were isolated, fed to an audio monitor and a window chronization responses elicited by these stimuli. discriminator (Frederick Haer and Co.), and displayed on a storage To elicit differential levels of EEG desynchronization, New oscilloscope. Two independent output channels of a Grass S88 stimu- Zealand rabbits were trained in a Pavlovian differential con- lator were used to administer the US to the pinna during behavioral ditioning paradigm in which a tone of one frequency, the CS+, conditioning and to produce anodal DC marker lesions (100 mA anodal was always followed by a brief electrical current applied to the DC for 5 set) at the end of selected, daily recording sessions. The EEG was amplified and recorded using Grass model 7P5 11 amplifiers and a pinna (i.e., the unconditional stimulus or US) and a tone of Grass model 78 polygraph. Neuronal responses, EEG, verbal commen- another frequency, the CS-, was never followed by the US. tary, and event markers were recorded on a multichannel FM tape Recent data from our laboratory have demonstrated that over recorder (A.R. Vetter Co.). The neuronal responses were fed into a the course ofconditioning significantly greater EEG desynchron- laboratorv minicomouter (ABLE 40. New England Diaital Co.) for on- line data -analysis. This computer also controlled the presentation of ization responses are elicited by the CS+ than by the CS-, stimuli during the conditioning procedure. The EEG was analyzed off reflecting a differentially conditioned change in the animal’s line by digitizing the taped signal using a sampling frequency of 128 Hz level of arousal to the presentation of these stimuli (Kapp et al., and subjecting it to a fast Fourier transformation using a Med Associates 199 1). Single neurons within the region of the NB were isolated data acquisition and fast Fourier analysis software package. and recorded (1) in response to CS+ and CS- presentations following the establishment of differentially conditioned EEG Behavioral training desynchronization responses, and (2) during stimulus-free pe- Following surgical recovery the animal was placed into the restrainer riods in order to determine correlations between their activity within the recording chamber for five, daily, 1 hr sessions, and the head and the magnitude of EEG desynchronization as determined by was immobilized by attachment of the nylon bolts to the modified fast Fourier transformation. stereotaxic frame. On the day following the last habituation session, a Pavlovian differential conditioning
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