Differential activation of fast-spiking and regular-firing neuron populations during movement and reward in the dorsal medial frontal cortex

Cerebral Cortex

Volumn 25, Issue 9, 2015, Pages 2631-2647

  Insel, Nathan ^a   Barnes, Carol A ^a,b  

^a 384 Life Sciences North Building   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Anterior cingulate cortex; Coding; Inhibition; Motivation; Rat

Indexed keywords

ANIMAL EXPERIMENT; ANTERIOR CINGULATE; ARTICLE; ASSOCIATION; AUDITORY STIMULATION; BRAIN CORTEX; CONTROLLED STUDY; DORSAL ANTERIOR CINGULATE CORTEX; DORSAL MEDIAL FRONTAL CORTEX; ELECTRIC POTENTIAL; FIRING RATE; MACHINE LEARNING; MALE; MEDIAL FRONTAL CORTEX; MOTIVATION; MOVEMENT (PHYSIOLOGY); NERVE CELL; NONHUMAN; PRELIMBIC CORTEX; PRIORITY JOURNAL; RAT; REWARD; SENSORY STIMULATION; SPIKE WAVE; TISSUE SECTION; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL; CLASSIFICATION; CYTOLOGY; DECISION MAKING; FISCHER 344 RAT; FRONTAL LOBE; NERVE CELL NETWORK; PHYSIOLOGY; REACTION TIME;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CHOICE BEHAVIOR; CUES; FRONTAL LOBE; MALE; MOVEMENT; NERVE NET; NEURONS; RATS; RATS, INBRED F344; REACTION TIME; REWARD;

EID: 84983341553     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu062     Document Type: Article

References (83)

1. Agmon A, Connors BW. 1992. Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci. 12:319-329.
2. Baeg EH, Kim YB, Jang J, Kim HT, Mook-Jung I, Jung MW. 2001. Fast spiking and regular spiking neural correlates of fear conditioning in the medial prefrontal cortex of the rat. Cereb Cortex. 11:441-451.
3. Barthó P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsáki G. 2004. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol. 92:600-608.
4. Benchenane K, Peyrache A, Khamassi M, Tierney PL, Gioanni Y, Battaglia FP, Wiener SI. 2010. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron. 66:921-936.
5. Birrell JM, Brown VJ. 2000. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci. 20:4320-4324.
6. Bock DD, Lee W-CA, Kerlin AM, Andermann ML, Hood G, Wetzel AW, Yurgenson S, Soucy ER, Kim HS, Reid RC. 2011. Network anatomy and in vivo physiology of visual cortical neurons. Nature. 471:177-182.
7. Buckley MJ, Mansouri FA, Hoda H, Mahboubi M, Browning PGF, Kwok SC, Phillips A, Tanaka K. 2009. Dissociable components of rule-guided behavior depend on distinct medial and prefrontal regions. Science. 325:52-58.
8. Buzsáki G. 1984. Feed-forward inhibition in the hippocampal formation. Prog Neurobiol. 22:131-153.
9. Buzsáki G, Eidelberg E. 1982. Direct afferent excitation and long-term potentiation of hippocampal interneurons. J Neurophysiol. 48:597-607.
10. Calvin WH, Sypert GW. 1976. Fast and slow pyramidal tract neurons: an intracellular analysis of their contrasting repetitive firing properties in the cat. J Neurophysiol. 39:420-434.
11. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai L-H, Moore CI. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature. 459:663-667.
12. Chagnac-Amitai Y, Luhmann HJ, Prince DA. 1990. Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J Comp Neurol. 296:598-613.
13. Chang Y-M, Luebke JI. 2007. Electrophysiological diversity of layer 5 pyramidal cells in the prefrontal cortex of the rhesus monkey: in vitro slice studies. J Neurophysiol. 98:2622-2632.
14. Chapin JK, Nicolelis MAL 1999. Principal component analysis of neuronal ensemble activity reveals multidimensional somatosensory representations. J Neurosci Methods. 94:121-140.
15. Connors BW, Gutnick MJ. 1990. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13:99-104.
16. Courtin J, Chaudun F, Rozeske RR, Karalis N, Gonzalez-Campo C, Wurtz H, Abdi A, Baufreton J, Bienvenu TCM, Herry C. 2014. Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature. 505:92-96.
17. Cowen SL, McNaughton BL. 2007. Selective delay activity in the medial prefrontal cortex of the rat: contribution of sensorimotor information and contingency. J Neurophysiol. 98:303-316.
18. Csicsvari J, Hirase H, Czurko A, Buzsáki G. 1998. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron. 21:179-189.
19. Curley AA, Lewis DA. 2012. Cortical basket cell dysfunction in schizophrenia. J Physiol. 590:715-724.
20. DeFelipe J, Hendry SHC, Jones EG. 1989. Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proc Natl Acad Sci USA. 86:2093-2097.
21. Dégenètais E, Thierry A-M, Glowinski J, Gioanni Y. 2002. Electrophysiological properties of pyramidal neurons in the rat prefrontal cortex: an in vivo intracellular recording study. Cereb Cortex. 12:1-16.
22. Durstewitz D, Vittoz NM, Floresco SB, Seamans JK. 2010. Abrupt transitions between prefrontal neural ensemble states accompany behavioral transitions during rule learning. Neuron. 66:438-448.
23. Eggermont JJ 1992. Neural interaction in cat primary auditory cortex. Dependence on recording depth, electrode separation, and age. J Neurophysiol. 68:1216-1228.
24. Eggermont JJ, Smith GM. 1996. Neural connectivity only accounts for a small part of neural correlation in auditory cortex. Exp Brain Res. 110:379-391.
25. Euston DR, Tatsuno M, McNaughton BL. 2007. Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science. 318:1147-1150.
26. Fox SE, Ranck JB Jr 1981. Electrophysiological characteristics of hippocampal complex-spike cells and theta cells. Exp Brain Res. 41:399-410.
27. Frankland PW, Bontempi B. 2005. The organization of recent and remote memories. Nat Rev Neurosci. 6:119-130.
28. Fujisawa S, Amarasingham A, Harrison MT, Buzsáki G. 2008. Behaviordependent short-term assembly dynamics in the medial prefrontal cortex. Nat Neurosci. 11:823-833.
29. Gao W-J, Zheng Z-H. 2004. Target-specific differences in somatodendritic morphology of layer V pyramidal neurons in rat motor cortex. J Comp Neurol. 476:174-185.
30. Guatteo E, Franceschetti S, Bacci A, Avanzini G, Wanke E. 1996. A TTX-sensitive conductance underlying burst firing in isolated pyramidal neurons from rat neocortex. Brain Res. 741:1-12.
31. Haddon JE, Killcross S. 2006. Both motivational and training factors affect response conflict choice performance in rats. Neural Netw. 19:1192-1202.
32. Haider B, Duque A, Hasenstaub AR, McCormick DA. 2006. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci. 26:4535-4545.
33. Hendry SHC, Jones EG, Emson PC, Lawson DEM, Heizmann CW, Streit P. 1989. Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res. 76:467-472.
34. Hillman KL, Bilkey DK. 2010. Neurons in the rat anterior cingulate cortex dynamically encode cost-benefit in a spatial decision-making task. J Neurosci. 30:7705-7713.
35. Hok V, Save E, Lenck-Santini PP, Poucet B. 2005. Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proc Natl Acad Sci USA. 102:4602-4607.
36. Hyman JM, Ma L, Balaguer-Ballester E, Durstewitz D, Seamans JK. 2012. Contextual encoding by ensembles of medial prefrontal cortex neurons. Proc Natl Acad Sci USA. 109:5086-5091.
37. Hyman JM, Whitman J, Emberly E, Woodward TS, Seamans JK. 2013. Action and outcome activity state patterns in the anterior cingulate cortex. Cereb Cortex. 23:1257-1268.
38. Insel N. 2010. Physiology of the medial frontal cortex during decisionmaking in adult and senescent rats (Ph.D.) [dissertation]. Tucson, AZ: University of Arizona. (p. 346).
39. Insel N, Patron LA, Hoang LT, Nematollahi S, Schimanski LA, Lipa P, Barnes CA. 2012. Reduced gamma frequency in the medial frontal cortex of aged rats during behavior and rest: implications for age-related behavioral slowing. J Neurosci. 32:16331-16344.
40. Insel N, Takehara-Nishiuchi K. 2013. The cortical structure of consolidated memory: a hypothesis on the role of the cingulate-entorhinal cortical connection. Neurobiol Learn Mem. 106:343-350.
41. Jay TM 2003. Dopamine: a potential substrate for synaptic plasticity and memory mechanisms. Prog Neurobiol. 69:375-390.
42. Karlsson MP, Tervo DGR, Karpova AY. 2012. Network resets in medial prefrontal cortex mark the onset of behavioral uncertainty. Science. 338:135-139.
43. Kawaguchi Y, Katsumaru H, Kosaka T, Heizmann CW, Hama K. 1987. Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res. 416:369-374.
44. Kawaguchi Y, Kubota Y. 1997. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex. 7:476-486.
45. Kehrer C, Maziashvili N, Dugladze T, Gloveli T. 2008. Altered excitatory-inhibitory balance in the NMDA-hypofunction model of schizophrenia. Front Mol Neurosci. 1:6.
46. Kennerley SW, Walton ME, Behrens TEJ, Buckley MJ, Rushworth MFS 2006. Optimal decision making and the anterior cingulate cortex. Nat Neurosci. 9:940-947.
47. Kim J, Ghim J-W, Lee JH, Jung MW. 2013. Neural correlates of interval timing in rodent prefrontal cortex. J Neurosci. 33: 13834-13847.
48. Kolling N, Behrens TEJ, Mars RB, Rushworth MFS 2012. Neural mechanisms of foraging. Science. 336:95-98.
49. Kvitsiani D, Ranade S, Hangya B, Taniguchi H, Huang JZ, Kepecs A. 2013. Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature. 498:363-366.
50. Lapish CC, Durstewitz D, Chandler LJ, Seamans JK. 2008. Successful choice behavior is associated with distinct and coherent network states in anterior cingulate cortex. Proc Natl Acad Sci USA. 105:11963-11968.
51. Laubach M, Shuler M, Nicolelis MAL 1999. Independent component analyses for quantifying neuronal ensemble interactions. J Neurosci Methods. 94:141-154.
52. Le Bé J-V, Silberberg G, Wang Y, Markram H. 2007. Morphological, electrophysiological, and synaptic properties of corticocallosal pyramidal cells in the neonatal rat neocortex. Cereb Cortex. 17:2204-2213.
53. Ma L, Hyman JM, Phillips AG, Seamans JK. 2014. Tracking progress toward a goal in corticostriatal ensembles. J Neurosci. 34:2244-2253.
54. Machens CK 2010. Demixing population activity in higher cortical areas. Front Comput Neurosci. 4:126.
55. McCormick DA, Connors BW, Lighthall JW, Prince DA. 1985. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol. 54:782-806.
56. Miller EK, Cohen JD. 2001. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 24:167-202.
57. Narayanan NS, Laubach M. 2009. Delay activity in rodent frontal cortex during a simple reaction time task. J Neurophysiol. 101: 2859-2871.
58. Nishimura Y, Asahi M, Saitoh K, Kitagawa H, Kumazawa Y, Itoh K, Lin M, Akamine T, Shibuya H, Asahara T et al. 2001. Ionic mechanisms underlying burst firing of layer III sensorimotor cortical neurons of the cat: an in vitro slice study. J Neurophysiol. 86:771-781.
59. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. 4th ed. San Diego: Academic Press.
60. Pi H-J, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A. 2013. Cortical interneurons that specialize in disinhibitory control. Nature. 503:521-524.
61. Pratt WE, Mizumori SJY 2001. Neurons in rat medial prefrontal cortex show anticipatory rate changes to predictable differential rewards in a spatial memory task. Behav Brain Res. 123:165-183.
62. Ragozzino ME, Kim J, Hassert D, Minniti N, Kiang C. 2003. The contribution of the rat prelimbic-infralimbic areas to different forms of task switching. Behav Neurosci. 117:1054-1065.
63. Rich EL, Shapiro M. 2009. Rat prefrontal cortical neurons selectively code strategy switches. J Neurosci. 29:7208-7219.
64. Rich EL, Shapiro ML. 2007. Prelimbic/infralimbic inactivation impairs memory for multiple task switches, but not flexible selection of familiar tasks. J Neurosci. 27:4747-4755.
65. Rigotti M, Barak O, Warden MR, Wang X-J, Daw ND, Miller EK, Fusi S. 2013. The importance of mixed selectivity in complex cognitive tasks. Nature. 497:585-590.
66. Robbins AA, Fox SE, Holmes GL, Scott RC, Barry JM. 2013. Short duration waveforms recorded extracellularly from freely moving rats are representative of axonal activity. Front Neural Circuits. 7:181.
67. Rubenstein JLR, Merzenich MM. 2003. Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav. 2:255-267.
68. Rushworth MFS, Walton ME, Kennerley SW, Bannerman DM. 2004. Action sets and decisions in the medial frontal cortex. Trends Cogn Sci. 8:410-417.
69. Sanchez-Vives MV, McCormick DA. 2000. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci. 3:1027-1034.
70. Schubert D, Staiger JF, Cho N, Kötter R, Zilles K, Luhmann HJ. 2001. Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J Neurosci. 21:3580-3592.
71. Shinomoto S, Kim H, Shimokawa T, Matsuno N, Funahashi S, Shima K, Fujita I, Tamura H, Doi T, Kawano K et al. 2009. Relating neuronal firing patterns to functional differentiation of cerebral cortex. PLoS Comput Biol. 5:e1000433.
72. Shu Y, Hasenstaub A, McCormick DA. 2003. Turning on and off recurrent balanced cortical activity. Nature. 423:288-293.
73. Sohal VS, Zhang F, Yizhar O, Deisseroth K. 2009. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature. 459:698-702.
74. Sul JH, Kim H, Huh N, Lee D, Jung MW. 2010. Distinct roles of rodent orbitofrontal and medial prefrontal cortex in decision making. Neuron. 66:449-460.
75. Sun YJ, Kim Y-J, Ibrahim LA, Tao HW, Zhang LI. 2013. Synaptic mechanisms underlying functional dichotomy between intrinsic-bursting and regular-spiking neurons in auditory cortical layer 5. J Neurosci. 33:5326-5339.
76. Swadlow HA 2003. Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex. 13:25-32.
77. Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RGM 2007. Schemas and memory consolidation. Science. 316:76-82.
78. White TD, Tan AM, Finch DM. 1990. Functional reciprocal connections of the rat entorhinal cortex and subicular complex with the medial frontal cortex: an in vivo intracellular study. Brain Res. 533:95-106.
79. Wilson MA, McNaughton BL. 1993. Dynamics of the hippocampal ensemble code for space. Science. 261:1055-1058.
80. Wilson NR, Runyan CA, Wang FL, Sur M. 2012. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature. 488:343-348.
81. Yang CR, Seamans JK, Gorelova N. 1996. Electrophysiological and morphological properties of layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro. J Neurosci. 16:1904-1921.
82. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT et al. 2011. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature. 477:171-178.
83. Zhu JJ, Connors BW. 1999. Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. J Neurophysiol. 81:1171-1183.