Immediate early gene fingerprints of multi-component behaviour.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
15 01 2020
15 01 2020
Historique:
received:
18
10
2019
accepted:
18
12
2019
entrez:
17
1
2020
pubmed:
17
1
2020
medline:
18
11
2020
Statut:
epublish
Résumé
The ability to execute different responses in an expedient temporal order is central for efficient goal-directed actions and often referred to as multi-component behaviour. However, the underlying neural mechanisms on a cellular level remain unclear. Here we establish a link between neural activity at the cellular level within functional neuroanatomical structures to this form of goal-directed behaviour by analyzing immediate early gene (IEG) expression in an animal model, the pigeon (Columba livia). We focus on the group of zif268 IEGs and ZENK in particular. We show that when birds have to cascade separate task goals, ZENK expression is increased in the avian equivalent of the mammalian prefrontal cortex, i.e. the nidopallium caudolaterale (NCL) as well as in the homologous striatum. Moreover, in the NCL as well as in the medial striatum (MSt), the degree of ZENK expression was highly correlated with the efficiency of multi-component behaviour. The results provide the first link between cellular IEG expression and behavioural outcome in multitasking situations. Moreover, the data suggest that the function of the fronto-striatal circuitry is comparable across species indicating that there is limited flexibility in the implementation of complex cognition such as multi-component behaviour within functional neuroanatomical structures.
Identifiants
pubmed: 31941919
doi: 10.1038/s41598-019-56998-4
pii: 10.1038/s41598-019-56998-4
pmc: PMC6962395
doi:
Substances chimiques
Early Growth Response Transcription Factors
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
384Commentaires et corrections
Type : ErratumIn
Références
Beste, C. et al. How minimal variations in neuronal cytoskeletal integrity modulate cognitive control. NeuroImage 185, 129–139 (2019).
pubmed: 30347280
Dippel, G. & Beste, C. A causal role of the right inferior frontal cortex in implementing strategies for multi-component behaviour. Nat. Commun. 6, 6587 (2015).
pubmed: 25850926
Duncan, J. The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn. Sci. 14, 172–179 (2010).
pubmed: 20171926
Mückschel, M., Stock, A.-K. & Beste, C. Psychophysiological mechanisms of interindividual differences in goal activation modes during action cascading. Cereb. Cortex N. Y. N 1991 24, 2120–2129 (2014).
Stock, A.-K., Arning, L., Epplen, J. T. & Beste, C. DRD1 and DRD2 genotypes modulate processing modes of goal activation processes during action cascading. J. Neurosci. Off. J. Soc. Neurosci. 34, 5335–5341 (2014).
Stock, A.-K., Gohil, K., Huster, R. J. & Beste, C. On the effects of multimodal information integration in multitasking. Sci. Rep. 7, 4927 (2017).
pubmed: 28687804
pmcid: 5501795
Gohil, K., Stock, A.-K. & Beste, C. The importance of sensory integration processes for action cascading. Sci. Rep. 5, 9485 (2015).
pubmed: 25820681
pmcid: 4377632
Beste, C. & Saft, C. Action selection in a possible model of striatal medium spiny neuron dysfunction: behavioral and EEG data in a patient with benign hereditary chorea. Brain Struct. Funct., https://doi.org/10.1007/s00429-013-0649-9 (2013).
Ness, V. & Beste, C. The role of the striatum in goal activation of cascaded actions. Neuropsychologia 51, 2562–2571 (2013).
pubmed: 24080261
Letzner, S., Güntürkün, O. & Beste, C. How birds outperform humans in multi-component behavior. Curr. Biol. CB 27, R996–R998 (2017).
pubmed: 28950092
Güntürkün, O. & Bugnyar, T. Cognition without Cortex. Trends Cogn. Sci. 20, 291–303 (2016).
pubmed: 26944218
Yildiz, A. et al. Feeling safe in the plane: neural mechanisms underlying superior action control in airplane pilot trainees–a combined EEG/MRS study. Hum. Brain Mapp. 35, 5040–5051 (2014).
pubmed: 24753040
pmcid: 4452896
Mückschel, M., Gohil, K., Ziemssen, T. & Beste, C. The norepinephrine system and its relevance for multi-component behavior. NeuroImage 146, 1062–1070 (2017).
pubmed: 27720820
Durstewitz, D., Kröner, S. & Güntürkün, O. The dopaminergic innervation of the avian telencephalon. Prog. Neurobiol. 59, 161–195 (1999).
pubmed: 10463794
Kröner, S. & Güntürkün, O. Afferent and efferent connections of the caudolateral neostriatum in the pigeon (Columba livia): a retro- and anterograde pathway tracing study. J. Comp. Neurol. 407, 228–260 (1999).
pubmed: 10213093
Kalenscher, T. et al. Neural correlates of a default response in a delayed go/no-go task. J. Exp. Anal. Behav. 84, 521–535 (2005).
pubmed: 16596978
pmcid: 1389779
Lengersdorf, D., Marks, D., Uengoer, M., Stüttgen, M. C. & Güntürkün, O. Blocking NMDA-receptors in the pigeon’s “prefrontal” caudal nidopallium impairs appetitive extinction learning in a sign-tracking paradigm. Front. Behav. Neurosci. 9 (2015).
Karakuyu, D., Herold, C., Güntürkün, O. & Diekamp, B. Differential increase of extracellular dopamine and serotonin in the ‘prefrontal cortex’ and striatum of pigeons during working memory: Monoamine homeostasis in the avian forebrain. Eur. J. Neurosci. 26, 2293–2302 (2007).
pubmed: 17908172
Waldmann, C. & Güntürkün, O. The dopaminergic innervation of the pigeon caudolateral forebrain: immunocytochemical evidence for a ‘prefrontal cortex’ in birds? Brain Res. 600, 225–234 (1993).
pubmed: 8435748
Diekamp, B., Kalt, T. & Güntürkün, O. Working memory neurons in pigeons. J. Neurosci. Off. J. Soc. Neurosci. 22, RC210 (2002).
Lengersdorf, D., Pusch, R., Güntürkün, O. & Stüttgen, M. C. Neurons in the pigeon nidopallium caudolaterale signal the selection and execution of perceptual decisions. Eur. J. Neurosci. 40, 3316–3327 (2014).
pubmed: 25146245
Puelles, L. et al. Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J. Comp. Neurol. 424, 409–438 (2000).
pubmed: 10906711
Güntürkün, O. The avian ‘prefrontal cortex’ and cognition. Curr. Opin. Neurobiol. 15, 686–693 (2005).
Kuenzel, W. J., Medina, L., Csillag, A., Perkel, D. J. & Reiner, A. The avian subpallium: New insights into structural and functional subdivisions occupying the lateral subpallial wall and their embryological origins. Brain Res. 1424, 67–101 (2011).
pubmed: 22015350
pmcid: 3378669
Reiner, A., Laverghetta, A. V., Meade, C. A., Cuthbertson, S. L. & Bottjer, S. W. An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch. J. Comp. Neurol. 469, 239–261 (2004).
pubmed: 14694537
Sheng, M. & Greenberg, M. E. The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4, 477–485 (1990).
pubmed: 1969743
Long, K. D. & Salbaum, J. M. Evolutionary conservation of the immediate-early gene ZENK. Mol. Biol. Evol. 15, 284–292 (1998).
pubmed: 9501495
Loebrich, S. & Nedivi, E. The Function of Activity-Regulated Genes in the Nervous System. Physiol. Rev. 89, 1079–1103 (2009).
pubmed: 19789377
pmcid: 2828052
Meyer, D. E. & Kieras, D. E. A computational theory of executive cognitive processes and multiple-task performance: Part 1. Basic mechanisms. Psychol. Rev. 104, 3–65 (1997).
pubmed: 9009880
Wu, C. & Liu, Y. Queuing network modeling of the psychological refractory period (PRP). Psychol. Rev. 115, 913–954 (2008).
pubmed: 18954209
Verbruggen, F., Schneider, D. W. & Logan, G. D. How to stop and change a response: the role of goal activation in multitasking. J. Exp. Psychol. Hum. Percept. Perform. 34, 1212–1228 (2008).
pubmed: 18823206
Shanahan, M., Bingman, V. P., Shimizu, T., Wild, M. & Güntürkün, O. Large-scale network organization in the avian forebrain: a connectivity matrix and theoretical analysis. Front. Comput. Neurosci. 7 (2013).
Vallortigara, G., Chiandetti, C. & Sovrano, V. A. Brain asymmetry (animal): Brain asymmetry. Wiley Interdiscip. Rev. Cogn. Sci. 2, 146–157 (2011).
pubmed: 26302006
Vallortigara, G. & Rogers, L. J. Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav. Brain Sci. 28, 575–589 (2005).
pubmed: 16209828
Diekamp, B., Regolin, L., Güntürkün, O. & Vallortigara, G. A left-sided visuospatial bias in birds. Curr. Biol. 15, R372–R373 (2005).
pubmed: 15916935
Xiao, Q. & Güntürkün, O. Asymmetrical Commissural Control of the Subdominant Hemisphere in Pigeons. Cell Rep. 25, 1171–1180.e3 (2018).
pubmed: 30380409
Van Ruijssevelt, L. et al. fMRI Reveals a Novel Region for Evaluating Acoustic Information for Mate Choice in a Female Songbird. Curr. Biol. 28, 711–721.e6 (2018).
pubmed: 29478859
Herold, C. et al. The receptor architecture of the pigeons’ nidopallium caudolaterale: an avian analogue to the mammalian prefrontal cortex. Brain Struct. Funct. 216, 239–254 (2011).
pubmed: 21293877
Kalt, T., Diekamp, B. & Güntürkün, O. Single unit activity during a Go/NoGo task in the “prefrontal cortex” of pigeons. Brain Res. 839, 263–278 (1999).
pubmed: 10519049
Gohil, K., Bluschke, A., Roessner, V., Stock, A.-K. & Beste, C. Sensory processes modulate differences in multi-component behavior and cognitive control between childhood and adulthood. Hum. Brain Mapp. 38, 4933–4945 (2017).
pubmed: 28660637
pmcid: 6867046
Bluschke, A., Gohil, K., Petzold, M., Roessner, V. & Beste, C. Neural mechanisms underlying successful and deficient multi-component behavior in early adolescent ADHD. NeuroImage Clin. 18, 533–542 (2018).
pubmed: 29560310
pmcid: 5857919
Kurzban, R., Duckworth, A., Kable, J. W. & Myers, J. An opportunity cost model of subjective effort and task performance. Behav. Brain Sci. 36 (2013).
Duncan, J. & Owen, A. M. Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci. 23, 475–483 (2000).
pubmed: 11006464
Anderson, K. D. & Reiner, A. Distribution and relative abundance of neurons in the pigeon forebrain containing somatostatin, neuropeptide Y, or both. J. Comp. Neurol. 299, 261–282 (1990).
pubmed: 1977774
Person, A. L., Gale, S. D., Farries, M. A. & Perkel, D. J. Organization of the songbird basal ganglia, including area X. J. Comp. Neurol. 508, 840–866 (2008).
pubmed: 18398825
Mezey, S. & Csillag, A. Selective striatal connections of midbrain dopaminergic nuclei in the chick (Gallus domesticus). Cell Tissue Res. 308, 35–46 (2002).
pubmed: 12012204
Albin, R. L., Young, A. B. & Penney, J. B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 12, 366–375 (1989).
pubmed: 2479133
Cui, G. et al. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494, 238–242 (2013).
pubmed: 23354054
pmcid: 4039389
Plenz, D. When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function. Trends Neurosci. 26, 436–443 (2003).
pubmed: 12900175
Bar-Gad, I., Morris, G. & Bergman, H. Information processing, dimensionality reduction and reinforcement learning in the basal ganglia. Prog. Neurobiol. 71, 439–473 (2003).
pubmed: 15013228
Humphries, M. D., Stewart, R. D. & Gurney, K. N. A Physiologically Plausible Model of Action Selection and Oscillatory Activity in the Basal Ganglia. J. Neurosci. 26, 12921–12942 (2006).
pubmed: 17167083
pmcid: 6674973
Redgrave, P., Vautrelle, N. & Reynolds, J. N. J. Functional properties of the basal ganglia’s re-entrant loop architecture: selection and reinforcement. Neuroscience 198, 138–151 (2011).
pubmed: 21821101
Yildiz, A. & Beste, C. Parallel and serial processing in dual-tasking differentially involves mechanisms in the striatum and the lateral prefrontal cortex. Brain Struct. Funct. 220, 3131–3142 (2015).
pubmed: 25017192
Graybiel, A. M. The Basal Ganglia and Chunking of Action Repertoires. Neurobiol. Learn. Mem. 70, 119–136 (1998).
pubmed: 9753592
Dubbeldam, J. L. & Den Boer-Visser, A. M. Organization of ‘feeding circuits’ in birds: pathways for the control of beak and head movements. Eur. J. Morphol. 32, 127–133 (1994).
pubmed: 7803158
Hellmann, B., Güntürkün, O. & Manns, M. Tectal mosaic: organization of the descending tectal projections in comparison to the ascending tectofugal pathway in the pigeon. J. Comp. Neurol. 472, 395–410 (2004).
pubmed: 15065115
Wild, J. M., Arends, J. J. A. & Zeigler, H. P. Telencephalic connections of the trigeminal system in the pigeon (Columba livia): A trigeminal sensorimotor circuit. J. Comp. Neurol. 234, 441–464 (1985).
pubmed: 3988994
Rose, J., Otto, T. & Dittrich, L. The Biopsychology-Toolbox: A free, open-source Matlab-toolbox for the control of behavioral experiments. J. Neurosci. Methods 175, 104–107 (2008).
pubmed: 18765252
Verbruggen, F. & Logan, G. D. Models of response inhibition in the stop-signal and stop-change paradigms. Neurosci. Biobehav. Rev. 33, 647–661 (2009).
pubmed: 18822313
Cole, A. J., Saffen, D. W., Baraban, J. M. & Worley, P. F. Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340, 474–476 (1989).
pubmed: 2547165
Stacho, M., Ströckens, F., Xiao, Q. & Güntürkün, O. Functional organization of telencephalic visual association fields in pigeons. Behav. Brain Res. 303, 93–102 (2016).
pubmed: 26802723
Mello, C. V. & Ribeiro, S. ZENK protein regulation by song in the brain of songbirds. J. Comp. Neurol. 393, 426–438 (1998).
pubmed: 9550149
Stacho, M., Letzner, S., Theiss, C., Manns, M. & Güntürkün, O. A GABAergic tecto-tegmento-tectal pathway in pigeons: The indirect tecto-tectal connection. J. Comp. Neurol. 524, 2886–2913 (2016).
pubmed: 26991544
Chi, V. & Chandy, K. G. Immunohistochemistry: Paraffin Sections Using the Vectastain ABC Kit from Vector Labs. J. Vis. Exp., https://doi.org/10.3791/308 (2007).
Nordmann, G. C. et al. A high sensitivity ZENK monoclonal antibody to map neuronal activity in Aves. Sci. Rep. (2020).
Wagenmakers, E.-J. A practical solution to the pervasive problems of p values. Psychon. Bull. Rev. 14, 779–804 (2007).
pubmed: 18087943
Kass, R. E. & Raftery, A. E. Bayes Factors. J. Am. Stat. Assoc. 90, 773–795 (1995).