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The Role of NMDA Receptors in the Pigeon Prefrontal Cortex

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The Role of NMDA Receptors in the Pigeon Prefrontal Cortex The role of NMDA receptors in the pigeon prefrontal cortex (Nidopallium caudolaterale) Inaugural - Dissertation zur Erlangung des Grades eines Doktors der Naturwissenschaften in der Fakultät für Psychologie der RUHR-UNIVERSITÄT BOCHUM vorgelegt von: Silke Lissek Mai 2004 Gedruckt mit Genehmigung der Fakultät für Psychologie der Ruhr-Universität Bochum. Referent: Prof. Dr. Dr. h.c. Onur Güntürkün Koreferent: Prof. Dr. Nikolaus Troje Tag der mündlichen Prüfung: 24. August 2004 TABLE OF CONTENTS 1. INTRODUCTION………………………………………………………… 1 1.1 Anatomy of the prefrontal cortex………………………………………….. 3 1.2 Pathophysiology of the frontal cortex / PFC in humans…………………… 5 1.3 Functional organization of the PFC ………………………………….……. 9 1.4 PFC and associative / extinction learning………………………………….. 10 1.5 PFC and short term / working memory……………………………………. 11 1.6 PFC and response inhibition……………………………………………….. 13 1.7 PFC and response selection………………………………………………… 15 1.8 PFC and context processing………………………………………………... 16 1.9 Properties of the NMDA receptor………………………………………….. 17 1.10 NMDA receptors (in PFC) and learning…………………………………… 21 1.11 NMDA receptors (in PFC) and short term / working memory…………….. 23 1.12 Interaction of glutamate / NMDA and DA in the PFC…………………….. 26 1.13 The pigeon Nidopallium caudolaterale (NCL)…………………………….. 29 1.14 NMDA receptors in avian brain and their role in learning…………..…….. 32 1.15 Aims of the present thesis………………………………………………….. 32 2. Dissociation of extinction and behavioral inhibition: the role of NMDA receptors in the pigeon associative forebrain during extinction………… 35 3. Maintenance in working memory or response selection? Functions of NMDA receptors in the pigeon "prefrontal cortex"…………………….. 42 4. Out of context – NMDA receptor antagonism in the avian “prefrontal cortex” impairs context processing in a conditional stimulus discrimination task………………………………………………………….. 53 5. GENERAL DISCUSSION…………………………………………………. 78 5.1 Extinction and behavioral inhibition………………………………………….. 79 5.2 Maintenance in working memory and response selection……………………. 82 5.3 Response selection from context or from reference memory………………… 88 5.4 How can NMDA receptor antagonism in the NCL influence learning and memory?……………………………………………………………………… 91 5.5 Comparison of lesions and D1 receptor blockade with NMDA receptor antagonism in NCL…………………………………………………………… 96 5.6 Summary Discussion of all results…………………………………………… 97 6. REFERENCES………………………………………………………………. 101 7. ATTACHMENTS …….…………………………………………………….. 132 TABLE OF CONTENTS 7.1 List of abbreviations.......................................................................................... 133 7.2 Illustration of the task used in Experiment 1 (Chapter 2)……………………………. 135 7.3 Illustration of the task used in Experiment 2 (Chapter 3)……………………………. 136 7.4 Positions of the cannulas for microinfusion into the NCL 137 7.5 Copy of the publication: Lissek S, Diekamp B & Güntürkün O (2002): Impaired learning of a color reversal task after NMDA receptor blockade in the pigeon (Columba livia) associative forebrain (Neostriatum Caudolaterale)………………… 138 CHAPTER 1: INTRODUCTION Chapter 1: Introduction 1 1. INTRODUCTION The prefrontal cortex (PFC) is a forebrain area in mammals crucial for integrating information from other brain regions in order to flexibly select and initiate behavior appropriate to the actual situation. It mediates input from higher order sensory and limbic areas, which describe and evaluate the situation in its relevant and irrelevant aspects, and motor output delivering the response appropriate to the actual situation. In order to be able to do this, the PFC subserves the functions of short term memory to maintain information relevant to the present task, and of working memory to manipulate this information. PFC is involved in learning processes, delivering flexible control over the connections between stimulus and response. Moreover, it is implicated in response selection, i.e. choosing of an adequate response with regard to the environmental conditions. For choosing a correct response, context processing is indispensable, meaning that PFC has to represent and consider all relevant information in the environment. Furthermore, PFC is involved in response inhibition, i.e. in suppression of inappropriate responses. Thus short term memory, working memory, associative learning, response selection, context processing and response inhibition are prerequisites of a functional PFC that altogether enable flexible adaptation of the organism to changing environmental conditions. NMDA receptors in various brain areas have been demonstrated to play a prominent role for learning and memory processes. As voltage- and ligand-dependent ion channels that open only if the presynaptic and postsynaptic neurons are activated simultaneously, their activation is a crucial step in the induction of long term potentiation (LTP) (Collingridge et al., 1983), which facilitates synaptic transmission and is thus considered the neural correlate of learning. A role for NMDA receptors in working memory is also discussed in neurocomputational studies. The mammalian brain possesses high densities of NMDA receptors, they are also abundant in PFC. As already demonstrated by several studies, they are presumably also involved in functions performed by PFC. The Nidopallium caudolaterale (NCL) is an associative area in the avian forebrain which is considered functionally equivalent to PFC in mammals based on neuroanatomical, behavioral, electrophysiological and microdialysis data. NMDA receptors are also found abundantly in NCL (Bock et al., 1997). Chapter 1: Introduction 2 A pilot study using blockade of NMDA receptors in the pigeon NCL (Lissek et al., 2002) demonstrated significant impairments in learning of a color reversal task. Due to the perseverative responding to the previously rewarded stimulus exhibited by the experimental group, the antagonist-treated animals needed significantly more trials than controls to learn the reversal. This deficit was particularly prominent during the first 2 reversal sessions, but performance differences remained also during the following 4 reversal sessions. The precise cause for the perseveration could not be detected in the scope of this task. Possible causes are deficits in extinction (refraining from responding to a no longer rewarded stimulus), impaired short term memory (no memory for the previous result of one’s own actions), impaired response inhibition (of a response detected as being inappropriate), deficits in response selection (from a repertoire of potentially correct responses) or a lack in context processing (insufficient consideration of the relevant information available in the task situation). Therefore, in this thesis, these prefrontal functions which might have contributed to the perseverative impairment shall be investigated separately in individual behavioral experiments using local blockade of NMDA receptors in the NCL. Experiment 1 (chapter 2) investigates the role of NMDA receptors in NCL for extinction learning and response inhibition. Experiment 2 (chapter 3) deals with the possible functions of NCL-based NMDA receptors for short term memory and response selection. Experiment 3 (chapter 4) studies the role of NMDA receptors in NCL for response selection and context processing. In the following sections, evidence for the abovementioned PFC-based functions, the role of NMDA receptors within the brain in general and within PFC in particular, as well as data on the NCL will be discussed in more detail. Afterwards, a rationale and an overview of the experiments conducted in the scope of this thesis will be presented. 1.1 Anatomy of the prefrontal cortex The human frontal lobes occupy almost a third of the cortical area in the human cerebral hemispheres. They can be subdivided into three main areas: motor-premotor areas (BA 4, 6, 8 and 44 according to the Brodmann nomenclature, 1909), paralimbic areas (BA 12, 24, Chapter 1: Introduction 3 25 and 32 located on the medial surface of the hemispheres), and heteromodal association cortex (BA 8, 9, 10, 11, 12, 32, 45, 46 and 47). The term prefrontal cortex refers almost exclusively to the paralimbic and heteromodal components of the frontal lobe (Mesulam, 2002). In humans, prefrontal cortex thus comprises all neocortical areas of the frontal lobe rostral to the premotor cortex up to the frontal pole. The heteromodal component is characterized by an isocortical architecture with high neuronal density, organized in six layers, while the paralimbic areas are characterized by a gradual transition from allocortex to isocortex, tending to have a lower neuronal density and less than six layers. The heteromodal component is commonly further subdivided into two main areas termed dorsolateral PFC (dlPFC) (BA 8, 9, 10, 44, 45, 46) and orbitofrontal cortex (OFC) (BA 11, 12 and 47) (Birbaumer, 1996). However, some researchers use a further distinction between dorsolateral PFC and ventrolateral PFC (vlPFC), the latter comprising the area of the inferior frontal gyrus and corresponding loosely to BA areas 44, 45 and 47 (Fletcher & Henson, 2001), while the former is assumed to correspond to BA 9 and 46. The PFC receives projections of the N. mediodorsalis of the thalamus (MD) (Rose & Woolsey, 1948; Divac et al., 1978), and from other thalamic nuclei and direct subcortical and limbic afferents from the pons, the tegmentum, the hypothalamus, and the amygdala (reviews in Fuster, 1989; Groenewegen, 1990). Moreover, there are afferents from hippocampus,
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