Sustained attentional states require distinct temporal involvement of the dorsal and ventral medial prefrontal cortex

Frontiers in Neural Circuits

Volumn 10, Issue AUG, 2016, Pages

  Luchicchi, Antonio ^a   Mnie Filali, Ouissame ^a   Terra, Huub ^a   Bruinsma, Bastiaan ^a   de Kloet, Sybren F ^a   Obermayer, Joshua ^a   Heistek, Tim S ^a   de Haan, Roel ^a   de Kock, Christiaan P J ^a   Deisseroth, Karl ^b   Pattij, Tommy ^c   Mansvelder, Huibert D ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b Stanford University   (United States)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Attention; Dorsomedial prefrontal cortex; Optogenetics; Pyramidal neurons; Ventromedial prefrontal cortex

Indexed keywords

ATTENTION; DISSOCIATION; DORSAL REGION; DORSOMEDIAL PREFRONTAL CORTEX; MEDIAL PREFRONTAL CORTEX; OPTOGENETICS; PYRAMIDAL NERVE CELL; STIMULUS; VENTROMEDIAL PREFRONTAL CORTEX; ANIMAL; ANIMAL BEHAVIOR; LONG EVANS RAT; MALE; PHYSIOLOGY; PREFRONTAL CORTEX; RAT;

ANIMALS; ATTENTION; BEHAVIOR, ANIMAL; MALE; OPTOGENETICS; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RATS; RATS, LONG-EVANS;

EID: 84989835872     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2016.00070     Document Type: Article

References (58)

1. Adhikari, A., Lerner, T. N., Finkelstein, J., Pak, S., Jennings, J. H., Davidson, T. J., et al. (2015). Basomedial amygdala mediates top-down control of anxiety and fear. Nature 527, 179–185. doi:10.1038/nature15698
2. Bari, A., Dalley, J. W., and Robbins, T. W. (2008). The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat. Protoc. 3, 759–767. doi:10.1038/nprot.2008.41
3. Broersen, L. M., and Uylings, H. B. (1999). Visual attention task performance in Wistar and Lister hooded rats: response inhibition deficits after medial prefrontal cortex lesions. Neuroscience 94, 47–57. doi:10.1016/S0306-4522(99)00312-7
4. Cassaday, H. J., Nelson, A. J. D., and Pezze, M. A. (2014). From attention to memory along the dorsal-ventral axis of the medial prefrontal cortex: some methodological considerations. Front. Syst. Neurosci. 8:160. doi:10.3389/fnsys.2014.00160
5. Cho, K. K. A., Hoch, R., Lee, A. T., Patel, T., Rubenstein, J. L. R., and Sohal, V. S. (2015). Gamma rhythms link prefrontal interneuron dysfunction with cognitive inflexibility in Dlx5/6(+/-) mice. Neuron 85, 1332–1343. doi:10.1016/j.neuron.2015.02.019
6. Chudasama, Y., and Muir, J. L. (2001). Visual attention in the rat: a role for the prelimbic cortex and thalamic nuclei? Behav. Neurosci. 115, 417–428. doi:10.1037/0735-7044.115.2.417
7. Chudasama, Y., Passetti, F., Rhodes, S. E. V., Lopian, D., Desai, A., and Robbins, T. W. (2003). Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity and compulsivity. Behav. Brain Res. 146, 105–119. doi:10.1016/j.bbr.2003.09.020
8. Dalley, J. W., Cardinal, R. N., and Robbins, T. W. (2004). Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci. Biobehav. Rev. 28, 771–784. doi:10.1016/j.neubiorev.2004.09.006
9. Delatour, B., and Gisquet-Verrier, P. (2001). Involvement of the dorsal anterior cingulate cortex in temporal behavioral sequencing: subregional analysis of the medial prefrontal cortex in rat. Behav. Brain Res. 126, 105–114. doi:10.1016/S0166-4328(01)00251-0
10. Delevich, K., Tucciarone, J., Huang, Z. J., and Li, B. (2015). The mediodorsal thalamus drives feedforward inhibition in the anterior cingulate cortex via parvalbumin interneurons. J. Neurosci. 35, 5743–5753. doi:10.1523/JNEUROSCI.4565-14.2015
11. Donnelly, N. A., Paulsen, O., Robbins, T. W., and Dalley, J. W. (2015). Ramping single unit activity in the medial prefrontal cortex and ventral striatum reflects the onset of waiting but not imminent impulsive actions. Eur. J. Neurosci. 41, 1524–1537. doi:10.1111/ejn.12895
12. Douglas, R. J., and Martin, K. C. (2004). Neuronal circuits of the neocortex. Annu. Rev. Neurosci. 27, 419–451. doi:10.1146/annurev.neuro.27.070203.144152
13. Feja, M., and Koch, M. (2014). Ventral medial prefrontal cortex inactivation impairs impulse control but does not affect delay-discounting in rats. Behav. Brain Res. 264, 230–239. doi:10.1016/j.bbr.2014.02.013
14. Gabbott, P. L. A., Warner, T. A., Jays, P. R. L., Salway, P., and Busby, S. J. (2005). Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol. 492, 145–177. doi:10.1002/cne.20738
15. Gisquet-Verrier, P., and Delatour, B. (2006). The role of the rat prelimbic/infralimbic cortex in working memory: not involved in the short-term maintenance but in monitoring and processing functions. Neuroscience 141, 585–596. doi:10.1016/j.neuroscience.2006.04.009
16. Gourley, S. L., and Taylor, J. R. (2016). Going and stopping: dichotomies in behavioral control by the prefrontal cortex. Nat. Neurosci. 19, 656–664. doi:10.1038/nn.4275
17. Granon, S., Hardouin, J., Courtièr, A., and Poucet, B. (1998). Evidence for the involvement of the rat prefrontal cortex in sustained attention. Q. J. Exp. Psychol. B 51, 219–233.
18. Gruber, A. J., Hussain, R. J., and O’donnell, P. (2009). The nucleus accumbens: a switchboard for goal-directed behaviors. PLoS ONE 4:e5062. doi:10.1371/journal.pone.0005062
19. Hayton, S. J., Lovett-Barron, M., Dumont, E. C., and Olmstead, M. C. (2010).Target-specific encoding of response inhibition: increased contribution of AMPA to NMDA receptors at excitatory synapses in the prefrontal cortex. J. Neurosci. 30, 11493–11500. doi:10.1523/JNEUROSCI.1550-10.2010
20. Heidbreder, C. A., and Groenewegen, H. J. (2003). The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neurosci. Biobehav. Rev. 27, 555–579. doi:10.1016/j.neubiorev.2003.09.003
21. Kahn, J. B., Ward, R. D., Kahn, L. W., Rudy, N. M., Kandel, E. R., Balsam, P. D., et al. (2012). Medial prefrontal lesions in mice impair sustained attention but spare maintenance of information in working memory. Learn. Mem. (Cold Spring Harbor, N.Y.) 19, 513–517. doi:10.1101/lm.026302.112
22. Kaping, D., Vinck, M., Hutchison, R. M., Everling, S., and Womelsdorf, T. (2011). Specific contributions of ventromedial, anterior cingulate, and lateral prefrontal cortex for attentional selection and stimulus valuation. PLoS Biol. 9:e1001224. doi:10.1371/journal.pbio.1001224
23. Kassam, S. M., Herman, P. M., Goodfellow, N. M., Alves, N. C., and Lambe, E. K. (2008). Developmental excitation of corticothalamic neurons by nicotinic acetylcholine receptors. J. Neurosci. 28, 8756–8764. doi:10.1523/JNEUROSCI.2645-08.2008
24. Killcross, S., and Coutureau, E. (2003). Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb. Cortex 13, 400–408. doi:10.1093/cercor/13.4.400
25. Kim, H., Ährlund-Richter, S., Wang, X., Deisseroth, K., and Carlén, M. (2016). Prefrontal parvalbumin neurons in control of attention. Cell 164, 208–218. doi:10.1016/j.cell.2015.11.038
26. Koike, H., Demars, M. P., Short, J. A., Nabel, E. M., Akbarian, S., Baxter, M. G., et al. (2015). Chemogenetic inactivation of dorsal anterior cingulate cortex neurons disrupts attentional behavior in mouse. Neuropsychopharmacology 41, 1014–1023. doi:10.1038/npp.2015.229
27. Miller, E. K., and Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202. doi:10.1146/annurev.neuro.24.1.167
28. Moore, T., Armstrong, K. M., and Fallah, M. (2003). Visuomotor origins of covert spatial attention. Neuron 40, 671–683. doi:10.1016/S0896-6273(03)00716-5
29. Muir, J. L., Everitt, B. J., and Robbins, T. W. (1996). The cerebral cortex of the rat and visual attentional function: dissociable effects of mediofrontal, cingulate, anterior dorsolateral, and parietal cortex lesions on a five-choice serial reaction time task. Cereb. Cortex 6, 470–481. doi:10.1093/cercor/6.3.470
30. Murphy, E. R., Fernando, A. B. P., Urcelay, G. P., Robinson, E. S. J., Mar, A. C., Theobald, D. E. H., et al. (2012). Impulsive behaviour induced by both NMDA receptor antagonism and GABAA receptor activation in rat ventromedial prefrontal cortex. Psychopharmacology 219, 401–410. doi:10.1007/s00213-011-2572-1
31. Niki, H., and Watanabe, M. (1979). Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Res. 171, 213–224. doi:10.1016/0006-8993(79)90328-7
32. Olton, D. S., Wenk, G. L., Church, R. M., and Meck, W. H. (1988). Attention and the frontal cortex as examined by simultaneous temporal processing. Neuropsychologia 26, 307–318. doi:10.1016/0028-3932(88)90083-8
33. Paine, T. A., Slipp, L. E., and Carlezon, W. A. Jr. (2011). Schizophrenia-like attentional deficits following blockade of prefrontal cortex GABAA receptors. Neuropsychopharmacology 36, 1703–1713. doi:10.1038/npp.2011.51
34. Park, J., Wood, J., Bondi, C., Del Arco, A., and Moghaddam, B. (2016). Anxiety evokes hypofrontality and disrupts rule-relevant encoding by dorsomedial prefrontal cortex neurons. J. Neurosci. 36, 3322–3335. doi:10.1523/JNEUROSCI.4250-15.2016
35. Parnaudeau, S., Taylor, K., Bolkan, S. S., Ward, R. D., Balsam, P. D., and Kellendonk, C. (2015). Mediodorsal thalamus hypofunction impairs flexible goal-directed behavior. Biol. Psychiatry 77, 445–453. doi:10.1016/j.biopsych.2014.03.020
36. Passetti, F., Chudasama, Y., and Robbins, T. W. (2002). The frontal cortex of the rat and visual attentional performance: dissociable functions of distinct medial prefrontal subregions. Cereb. Cortex 12, 1254–1268. doi:10.1093/cercor/12.12.1254
37. Paxinos, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates. London: Elsevier Academic Press.
38. Petrides, M. (2000). Dissociable roles of mid-dorsolateral prefrontal and anterior inferotemporal cortex in visual working memory. J. Neurosci. 20, 7496–7503.
39. Pezze, M., McGarrity, S., Mason, R., Fone, K. C., and Bast, T. (2014). Too little and too much: hypoactivation and disinhibition of medial prefrontal cortex cause attentional deficits. J. Neurosci. 34, 7931–7946. doi:10.1523/JNEUROSCI.3450-13.2014
40. Pinto, L., Goard, M. J., Estandian, D., Xu, M., Kwan, A. C., Lee, S.-H., et al. (2013). Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat. Neurosci. 16, 1857–1863. doi:10.1038/nn.3552
41. Pragay, E. B., Mirsky, A. F., and Nakamura, R. K. (1987). Attention- related unit activity in the frontal association cortex during a go/no-go visual discrimination task. Exp. Neurol. 96, 481–500. doi:10.1016/0014-4886(87)90213-5
42. Proulx, E., Piva, M., Tian, M. K., Bailey, C. D. C., and Lambe, E. K. (2014). Nicotinic acetylcholine receptors in attention circuitry: the role of layer VI neurons of prefrontal cortex. Cell. Mol. Life Sci. 71, 1225–1244. doi:10.1007/s00018-013-1481-3
43. Riga, D., Matos, M. R., Glas, A., Smit, A. B., Spijker, S., and Van Den Oever, M. C. (2014). Optogenetic dissection of medial prefrontal cortex circuitry. Front. Syst. Neurosci. 8:230. doi:10.3389/fnsys.2014.00230
44. Risterucci, C., Terramorsi, D., Nieoullon, A., and Amalric, M. (2003). Excitotoxic lesions of the prelimbic-infralimbic areas of the rodent prefrontal cortex disrupt motor preparatory processes. Eur. J. Neurosci. 17, 1498–1508. doi:10.1046/j.1460-9568.2003.02541.x
45. Robbins, T. W. (2002). The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology 163, 362–380. doi:10.1007/s00213-002-1154-7
46. Rodgers, C. C., and Deweese, M. R. (2014). Neural correlates of task switching in prefrontal cortex and primary auditory cortex in a novel stimulus selection task for rodents. Neuron 82, 1157–1170. doi:10.1016/j.neuron.2014.04.031
47. Romanski, L. M., Tian, B., Fritz, J., Mishkin, M., Goldman-Rakic, P. S., and Rauschecker, J. P. (1999). Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat. Neurosci. 2, 1131–1136. doi:10.1038/16056
48. Semenova, S., Stolerman, I. P., and Markou, A. (2007). Chronic nicotine administration improves attention while nicotine withdrawal induces performance deficits in the 5-choice serial reaction time task in rats. Pharmacol. Biochem. Behav. 87, 360–368. doi:10.1016/j.pbb.2007.05.009
49. Sesack, S. R., Deutch, A. Y., Roth, R. H., and Bunney, B. S. (1989). Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol. 290, 213–242. doi:10.1002/cne.902900205
50. Smith, K. S., Virkud, A., Deisseroth, K., and Graybiel, A. M. (2012). Reversible online control of habitual behavior by optogenetic perturbation of medial prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 109, 18932–18937. doi:10.1073/pnas.1216264109
51. Thomson, A. M. (2010). Neocortical layer 6, a review. Front. Neuroanat. 4:13. doi:10.3389/fnana.2010.00013
52. Totah, N. K. B., Jackson, M. E., and Moghaddam, B. (2013). Preparatory attention relies on dynamic interactions between prelimbic cortex and anterior cingulate cortex. Cereb. Cortex 23, 729–738. doi:10.1093/cercor/bhs057
53. Totah, N. K. B., Kim, Y. B., Homayoun, H., and Moghaddam, B. (2009). Anterior cingulate neurons represent errors and preparatory attention within the same behavioral sequence. J. Neurosci. 29, 6418–6426. doi:10.1523/JNEUROSCI.1142-09.2009
54. van Aerde, K. I., Heistek, T. S., and Mansvelder, H. D. (2008). Prelimbic and infralimbic prefrontal cortex interact during fast network oscillations. PLoS ONE 3:e2725. doi:10.1371/journal.pone.0002725
55. Wimmer, R. D., Schmitt, L. I., Davidson, T. J., Nakajima, M., Deisseroth, K., and Halassa, M. M. (2015). Thalamic control of sensory selection in divided attention. Nature 526, 705–709. doi:10.1038/nature15398
56. Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M., and Deisseroth, K. (2011). Optogenetics in neural systems. Neuron 71, 9–34. doi:10.1016/j.neuron.2011.06.004
57. Zhang, S., Xu, M., Kamigaki, T., Hoang Do, J. P., Chang, W.-C., Jenvay, S., et al. (2014). Selective attention. Long-range and local circuits for top- down modulation of visual cortex processing. Science 345, 660–665. doi:10.1126/science.1254126
58. Zingg, B., Hintiryan, H., Gou, L., Song, M. Y., Bay, M., Bienkowski, M. S., et al. (2014). Neural networks of the mouse neocortex. Cell 156, 1096–1111. doi:10.1016/j.cell.2014.02.023