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Parietal Neurophysiology During Sustained Attentional Performance: Assessment of Cholinergic Contribution to Parietal Processing

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Parietal Neurophysiology During Sustained Attentional Performance: Assessment of Cholinergic Contribution to Parietal Processing PARIETAL NEUROPHYSIOLOGY DURING SUSTAINED ATTENTIONAL PERFORMANCE: ASSESSMENT OF CHOLINERGIC CONTRIBUTION TO PARIETAL PROCESSING DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of the Ohio State University By John Isaac Broussard, B.A., M.A. **** The Ohio State University 2007 Dissertation Committee: Approved by Associate Professor Ben Givens, Advisor Professor Martin Sarter Professor John Bruno ______________________________ Associate Professor John Buford Advisor Graduate Program in Psycholology ABSTRACT There were three major aims of this dissertation, all of which pertained to neurophysiological correlates of sustained attention task performance in rats. The first aim was to examine whether the evoked neurophysiological responses of local field potential activity of the parietal cortex during the detection of signals and the rejection of nonsignals produces behavioral correlates similar to that of single unit activity. The second aim was to test whether removal of local cholinergic input to the PPC via infusion of a specific cholinotoxin reduces the signal-related increases in firing rate of PPC neurons. The third aim was to test whether unilateral cholinergic deafferentation of the medial prefrontal cortex of rats specifically reduced the responses of PPC in the presence of a visual distractor. In the first study, it was determined that visual signal recruited an event-related potential (ERP) similar to the P300, an ERP component found in human PPC during the detection of infrequent and unpredictable stimuli. Amplitude of the ERP varied as a function of signal duration. Analysis of the spectral content of the evoked response indicated increases in alpha power as a function of correct detection. In the second study it was determined that restricted loss of cholinergic input near the recording site significantly reduced the relative number of signal-related neurons in the PPC. This manipulation also increased the relative number of neurons responsive to the visual distractor, and increased the baseline firing rate of neurons initially activated by the signal. In the third study cholinergic ii deafferentation of mPFC did not reduce the number of neurons responsive to the visual signal, but analysis of the trial blocks indicated a specific impairment of these neurons to encode the signal in the presence of the distractor. Further, bilateral cholinergic deafferentation produced a side bias to the hit lever during distractor sessions. The results of these experiments suggest that cholinergic input to the PPC is necessary for the filtering of distractors and the optimization of signal-related activity, whereas cholinergic input to the mPFC of rats is specifically required to produce the behavioral flexibility to maintain task performance under attentional challenges. iii Dedicated to Yun-ju iv ACKNOWLEDGEMENTS I would like to express my appreciation to my advisor, Ben Givens, for patience and encouragement throughout my graduate career. I thank Martin Sarter, who provided guidance and intellectual stimulation at every encounter. John Bruno has shared much knowledge and wisdom, and has helped me develop my skills as a writer and a presenter with useful classes and advice over the years. I am grateful to John Buford for his participation in this committee. Special thanks are due to past and current students and post-doctoral associates. Mike Gill was always quick to respond to my many, many technical inquiries early in my tenure here. Josh Burke and Chris Herzog were also very supportive for my first year. Sharmila Venugopal’s contribution in aiding the programming and calibration of the hardware and software was invaluable. I thank Kate Karelina for her assistance with technical aspects of these experiments. The many undergraduates who have contributed their time and effort have been invaluable in my studies. A short list includes: Michael Rosner, David Osher, Andrea Kornbau, Karen Lindsay, Celia Less, Tim, Sameh Elguizaoui, Sara Shelton, Ryan Dagg, Timothy Simmons, Amy Gosnell, and Amir Adeli. v VITA December 05, 1978………………………Born – Abbeville, Louisiana 2001……………………………………...B.S. Psychology, Louisiana State University. 2004……………………………………...M.A. Psychology The Ohio State University. 2001-present…………………………….Graduate Teaching and Research Associate, The Ohio State University PUBLICATIONS 1. Broussard, J., Sarter, M., & Givens, B. (2006). Neuronal correlates of signal detection in the posterior parietal cortex of rats performing a sustained attention task. Neuroscience. 143: 2, 407-417. 2. Hawkins, M.F., Uzelac, S.M., Baumeister, A.A., Hearn, J.K., Broussard, J.I., & Guillot, T.S. (2002). Behavioral Responses to Stress Following Central and Peripheral Injection of the 5-HT2 Agonist DOI. Pharmacology, Biochemistry, & Behavior. 73: 3, 537-544. FIELDS OF STUDY Major Field: Psychology Minor Field: Behavioral Neuroscience vi TABLE OF CONTENTS Abstract……………………………………………………………………………...........ii Dedication……………………………………………………………………….………..iv Acknowledgements………………………………………………………………………..v Vita……………………………………………………………………..............................vi List of Tables………………………………………………………………………...........x List of Figures…………………………………………………………………………….xi 1. General Introduction………………………………………………………………..…..1 1.1. Posterior parietal cortex contributes to attentional processing……………….1 1.2 Identification of the rodent homologue of the PPC…………………………...4 1.3 The role of ACh in the evoked response……………………………………...6 1.4 ACh input in cortical synchrony………………………………………..……12 1.5 Frontal cortex and effortful cognitive control…………………………..……16 1.6 Specific Aims ………………………….………………………………........19 2. General Methods……………………………………………………………………...24 2.1 Subjects and apparatus……………………………………………………….24 2.2. Behavioral training…………………………………………………………..25 2.3. Electrode and infusion cannula implantation………………………………..27 2.4. Neurophysiological recording sessions……………………………………...28 2.5. Histology………………………………………………………………….....29 2.6. Behavioral measures………………………………………………………...30 2.7. Neurophysiological measures……………………………………………….31 3. Experiment One………………………………………………………………….……34 3.1. Introduction………………………………………………………………....34 3.2. Specific Methods…………………………………………………………....39 3.2.1. Recording and analysis of EEG…………………………………...39 3.3. Results………………………………………………………………….……41 3.3.1. Histology…………………………………………………….…….41 3.3.2. Behavioral effects of signal duration and distractor………………41 3.3.3. Event Related Potentials…………………………………………..42 3.3.4. Increases in delta and theta power reflect changes in signal duration…………………………………………………43 3.3.5. Phasic increases in alpha power reflect correct detection of signals ………………………………………………………...44 vii 3.3.6. Distractor evoked changes in phasic and tonic alpha power ………………………………………………………..…..45 3.4. Discussion………………………………………………………………...…46 3.4.1. Evoked P300 response and lower frequency oscillations………....46 3.4.2. Phasic Increases in the alpha power as a function of correct detection………………………………………………………….47 3.4.3. Tonic levels of alpha power: a marker of attentional effort?...........48 3.4.4. Distinctions between LFP and Single Unit Activity…….…….....49 3.4.5. Duration- and detection- related changes in the evoked potentials.51 3.4.6. Cholinergic input and the production of theta and alpha rhythms..52 3.4.7. Parietal functions in visual attention performance of rats………...53 4. Experiment two………………………………………………………………….........66 4.1. Introduction…………………………………………………………………66 4.2. Specific Methods……………………………………………….........……...68 4.2.1 Electrode and infusion cannula implantation……………………....68 4.2.2 Neurophysiological recording sessions…………………………….68 4.3. Results………………………………………………………….…………...70 4.3.1. Histology………………………………..........................................70 4.3.2. Behavioral performance under standard and distractor conditions…………………………...….…………...…71 4.3.3. Significant activation of PPC neuronal activity during the detection of signals……………………....……...........72 4.3.4. Effects of signal duration on signal-evoked PPC activity.……….73 4.3.5. Distractor-induced modulation of signal-evoked activation of PPC neurons………………………………….……74 4.3.6. Cholinergic deafferentation increased distractor-related PPC unit activity……………………...........................................75 4.3.7. Cholinergic deafferentation reduced signal-evoked PPC unit activity ………………………………………………….….75 4.3.8. Cholinergic modulation of the SNR under attentionally challenging conditions………………………………………………………..76 4.3.9 Correct versus incorrect trials…………………………………….78 4.4. Discussion…………………………………………………………………..78 4.4.1. Effects of signal duration and distractor……………………...…..79 4.4.2. Cholinergic modulation of PPC function in rats………………....80 4.4.3. Cholinergic modulation of signal-evoked activity…………….…80 4.4.4. Cholinergic suppression of distractor-related activity…………...81 5. Experiment three………………………………………………………………………97 viii 5.1. Introduction………………………………………………………………….97 5.2. Specific Methods…………………………………………………………..102 5.2.1. Subjects…………………………………………………………..102 5.2.2. Surgery………………………………………………………..…103 5.2.3. Histology………………………………………………………..104 5.2.4. Behavioral Measures……………………………………………104 5.2.5. Neurophysiological Measures………………………………….105 5.3. Results……………………………………………………………………..105 5.3.1. Effects of response cost and time outs on premature responding..105 5.3.2. Histology…………………………………………………………106 5.3.3. Initial lesions do not impair behavioral performance ...…………107 5.3.4. Bilateral lesions increase
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