Dynamic Changes in Single Unit Activity and Gamma Oscillations in a Thalamocortical Circuit during Rapid Instrumental Learning

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Yu, Chunxiu ^a   Fan, David ^a   Lopez, Alberto ^a   Yin, Henry H ^a,b  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL CELL; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTRODE; ELECTROENCEPHALOGRAM; FEEDBACK SYSTEM; GAMMA OSCILLATION; GAMMA RHYTHM; LEARNING; MALE; NERVE CELL; NONHUMAN; OSCILLATION; RAT; REINFORCEMENT; REWARD; SPIKE; SPIKE WAVE; THALAMOCORTICAL TRACT; THETA RHYTHM; VENTROMEDIAL PREFRONTAL CORTEX;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN WAVES; CONDITIONING, OPERANT; ELECTRODES; LONG-TERM POTENTIATION; MALE; NERVE NET; NEURONS; PREFRONTAL CORTEX; RATS; THALAMUS; TIME FACTORS;

RATTUS;

EID: 84870603204     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050578     Document Type: Article

References (58)

1. Miller EK, (2000) The prefrontal cortex and cognitive control. Nat Rev Neurosci 1: 59-65.
2. Matsumoto K, Suzuki W, Tanaka K, (2003) Neuronal correlates of goal-based motor selection in the prefrontal cortex. Science 301: 229-232.
3. Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S, (2004) The role of the medial frontal cortex in cognitive control. Science 306: 443-447.
4. Corbit LH, Muir JL, Balleine BW, (2003) Lesions of mediodorsal thalamus and anterior thalamic nuclei produce dissociable effects on instrumental conditioning in rats. Eur J Neurosci 18: 1286-1294.
5. Goldman-Rakic PS, Porrino LJ, (1985) The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J Comp Neurol 242: 535-560.
6. Giguere M, Goldman-Rakic PS, (1988) Mediodorsal nucleus: areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys. J Comp Neurol 277: 195-213.
7. Groenewegen HJ, (1988) Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neuroscience 24: 379-431.
8. Ray JP, Price JL, (1992) The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain-prefrontal cortex topography. J Comp Neurol 323: 167-197.
9. Ray JP, Price JL, (1993) The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 337: 1-31.
10. Pirot S, Jay TM, Glowinski J, Thierry AM, (1994) Anatomical and electrophysiological evidence for an excitatory amino acid pathway from the thalamic mediodorsal nucleus to the prefrontal cortex in the rat. Eur J Neurosci 6: 1225-1234.
11. Kuroda M, Yokofujita J, Murakami K, (1998) An ultrastructural study of the neural circuit between the prefrontal cortex and the mediodorsal nucleus of the thalamus. Prog Neurobiol 54: 417-458.
12. Floresco SB, Grace AA, (2003) Gating of hippocampal-evoked activity in prefrontal cortical neurons by inputs from the mediodorsal thalamus and ventral tegmental area. J Neurosci 23: 3930-3943.
13. Ferron A, Thierry AM, Le Douarin C, Glowinski J, (1984) Inhibitory influence of the mesocortical dopaminergic system on spontaneous activity or excitatory response induced from the thalamic mediodorsal nucleus in the rat medial prefrontal cortex. Brain Res 302: 257-265.
14. Herry C, Vouimba RM, Garcia R, (1999) Plasticity in the mediodorsal thalamo-prefrontal cortical transmission in behaving mice. J Neurophysiol 82: 2827-2832.
15. McDonald AJ, (1991) Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44: 1-14.
16. Maurice N, Deniau JM, Glowinski J, Thierry AM, (1998) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J Neurosci 18: 9539-9546.
17. Maurice N, Deniau JM, Menetrey A, Glowinski J, Thierry AM, (1998) Prefrontal cortex-basal ganglia circuits in the rat: involvement of ventral pallidum and subthalamic nucleus. Synapse 29: 363-370.
18. Yin HH, Knowlton BJ, (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7: 464-476.
19. Haber SN, Calzavara R, (2009) The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull 78: 69-74.
20. Rushworth MF, Noonan MP, Boorman ED, Walton ME, Behrens TE, (2011) Frontal cortex and reward-guided learning and decision-making. Neuron 70: 1054-1069.
21. Gaffan D, Murray EA, (1990) Amygdalar interaction with the mediodorsal nucleus of the thalamus and the ventromedial prefrontal cortex in stimulus-reward associative learning in the monkey. J Neurosci 10: 3479-3493.
22. Hunt PR, Aggleton JP, (1998) Neurotoxic lesions of the dorsomedial thalamus impair the acquisition but not the performance of delayed matching to place by rats: a deficit in shifting response rules. J Neurosci 18: 10045-10052.
23. Mitchell AS, Baxter MG, Gaffan D, (2007) Dissociable performance on scene learning and strategy implementation after lesions to magnocellular mediodorsal thalamic nucleus. J Neurosci 27: 11888-11895.
24. Mitchell AS, Browning PG, Baxter MG, (2007) Neurotoxic lesions of the medial mediodorsal nucleus of the thalamus disrupt reinforcer devaluation effects in rhesus monkeys. J Neurosci 27: 11289-11295.
25. Ostlund SB, Balleine BW, (2008) Differential involvement of the basolateral amygdala and mediodorsal thalamus in instrumental action selection. J Neurosci 28: 4398-4405.
26. Balleine BW, Dickinson A, (1998) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37: 407-419.
27. Killcross S, Coutureau E, (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13: 400-408.
28. Corbit LH, Balleine BW, (2003) The role of prelimbic cortex in instrumental conditioning. Behav Brain Res 146: 145-157.
29. Haddon JE, Killcross S, (2006) Prefrontal cortex lesions disrupt the contextual control of response conflict. J Neurosci 26: 2933-2940.
30. Hadland KA, Rushworth MF, Gaffan D, Passingham RE, (2003) The anterior cingulate and reward-guided selection of actions. J Neurophysiol 89: 1161-1164.
31. Adams CD, Dickinson A, (1981) Instrumental responding following reinforcer devaluation. Quarterly Journal of Experimental Psychology 33: 109-122.
32. Fan D, Rossi MA, Yin HH, (2012) Mechanisms of action selection and timing in substantia nigra neurons. J Neurosci 32: 5534-5548.
33. Fan D, Rich D, Holtzman T, Ruther P, Dalley JW, et al. (2011) A wireless multi-channel recording system for freely behaving mice and rats. PLoS One 6: e22033.
34. Pereda E, Quiroga RQ, Bhattacharya J, (2005) Nonlinear multivariate analysis of neurophysiological signals. Prog Neurobiol 77: 1-37.
35. Sakkalis V, Doru Giurc Neanu C, Xanthopoulos P, Zervakis ME, Tsiaras V, et al. (2009) Assessment of linear and nonlinear synchronization measures for analyzing EEG in a mild epileptic paradigm. IEEE Trans Inf Technol Biomed 13: 433-441.
36. Dickinson A, (1985) Actions and habits: the development of behavioural autonomy. Philosophical Transactions of the Royal Society B308: 67-78.
37. Buzsaki G, Anastassiou CA, Koch C, (2012) The origin of extracellular fields and currents- EEG, ECoG, LFP and spikes. Nat Rev Neurosci 13: 407-420.
38. Basar E, Basar-Eroglu C, Karakas S, Schurmann M, (2000) Brain oscillations in perception and memory. Int J Psychophysiol 35: 95-124.
39. Buzsaki G, Wang XJ (2012) Mechanisms of Gamma Oscillations. Annu Rev Neurosci.
40. van der Meer MA, Redish AD, (2009) Low and High Gamma Oscillations in Rat Ventral Striatum have Distinct Relationships to Behavior, Reward, and Spiking Activity on a Learned Spatial Decision Task. Front Integr Neurosci 3: 9.
41. Berke JD, Okatan M, Skurski J, Eichenbaum HB, (2004) Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 43: 883-896.
42. DeCoteau WE, Thorn C, Gibson DJ, Courtemanche R, Mitra P, et al. (2007) Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task. Proc Natl Acad Sci U S A 104: 5644-5649.
43. Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, et al. (2010) Coherent theta oscillations and reorganization of spike timing in the hippocampal- prefrontal network upon learning. Neuron 66: 921-936.
44. Fries P, Reynolds JH, Rorie AE, Desimone R, (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291: 1560-1563.
45. Hasselmo ME, (2005) What is the function of hippocampal theta rhythm?-Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 15: 936-949.
46. Benchenane K, Tiesinga PH, Battaglia FP, (2011) Oscillations in the prefrontal cortex: a gateway to memory and attention. Curr Opin Neurobiol 21: 475-485.
47. van der Meer MA, Redish AD, (2009) Covert Expectation-of-Reward in Rat Ventral Striatum at Decision Points. Front Integr Neurosci 3: 1.
48. Jones MW, Wilson MA, (2005) Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol 3: e402.
49. Lee H, Simpson GV, Logothetis NK, Rainer G, (2005) Phase locking of single neuron activity to theta oscillations during working memory in monkey extrastriate visual cortex. Neuron 45: 147-156.
50. Cashdollar N, Malecki U, Rugg-Gunn FJ, Duncan JS, Lavie N, et al. (2009) Hippocampus-dependent and-independent theta-networks of active maintenance. Proc Natl Acad Sci U S A 106: 20493-20498.
51. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24: 49-65, 111-125.
52. Varela F, Lachaux JP, Rodriguez E, Martinerie J, (2001) The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2: 229-239.
53. Grillner S, Hellgren J, Menard A, Saitoh K, Wikstrom MA (2005) Mechanisms for selection of basic motor programs- roles for the striatum and pallidum. Trends Neurosci.
54. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW, (2005) The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22: 513-523.
55. Luk CH, Wallis JD, (2009) Dynamic encoding of responses and outcomes by neurons in medial prefrontal cortex. J Neurosci 29: 7526-7539.
56. Yu C, Gupta J, Yin HH (2010) The role of mediodorsal thalamus in temporal differentiation of reward-guided actions. Front Integr Neurosci 4.
57. Ostlund SB, Balleine BW, (2005) Lesions of medial prefrontal cortex disrupt the acquisition but not the expression of goal-directed learning. J Neurosci 25: 7763-7770.
58. Paxinos G, Watson C (1998) The rat brain in sterotaxic coordinates. San Diego: Academic Press.