Top

Published in:

Open Access 01-09-2017 | Original Article

Altered cortico-striatal crosstalk underlies object recognition memory deficits in the sub-chronic phencyclidine model of schizophrenia

Authors: Aman Asif-Malik, Daniel Dautan, Andrew M. J. Young, Todor V. Gerdjikov

Published in: Brain Structure and Function | Issue 7/2017

Abstract

The neural mechanisms underlying cognitive deficits in schizophrenia are poorly understood. Sub-chronic treatment with the NMDA antagonist phencyclidine (PCP) produces cognitive abnormalities in rodents that reliably model aspects of the neurocognitive alterations observed in schizophrenia. Given that network activity across regions encompassing medial prefrontal cortex (mPFC) and nucleus accumbens (NAc) plays a significant role in motivational and cognitive tasks, we measured activity across cortico-striatal pathways in PCP-treated rats to characterize neural enabling and encoding of task performance in a novel object recognition task. We found that PCP treatment impaired task performance and concurrently (1) reduced tonic NAc neuronal activity, (2) desynchronized cross-activation of mPFC and NAc neurons, and (3) prevented the increase in mPFC and NAc neural activity associated with the exploration of a novel object in relation to a familiar object. Taken together, these observations reveal key neuronal and network-level adaptations underlying PCP-induced cognitive deficits, which may contribute to the emergence of cognitive abnormalities in schizophrenia.

Agmon A (2012) A novel, jitter-based method for detecting and measuring spike synchrony and quantifying temporal firing precision. Neural Syst Circuits. doi:10.1186/2042-1001-2-5 PubMedPubMedCentral

Akirav I, Maroun M (2006) Ventromedial prefrontal cortex is obligatory for consolidation and reconsolidation of object recognition memory. Cereb Cortex 16(12):1759–1765. doi:10.1093/cercor/bhj114 CrossRefPubMed

an der Heiden W, Hafner H (2000) The epidemiology of onset and course of schizophrenia. Eur Arch Psychiatry Clin Neurosci 250(6):292–303CrossRef

Bado P, Madeira C, Vargas-Lopes C, Moulin TC, Wasilewska-Sampaio AP, Maretti L, de Oliveira RV, Amaral OB, Panizzutti R (2011) Effects of low-dose D-serine on recognition and working memory in mice. Psychopharmacology (Berl) 218(3):461–470. doi:10.1007/s00213-011-2330-4 CrossRef

Barker GR, Warburton EC (2011) When is the hippocampus involved in recognition memory? J Neurosci 31(29):10721–10731. doi:10.1523/JNEUROSCI.6413-10.2011 CrossRefPubMed

Barker GR, Bird F, Alexander V, Warburton EC (2007) Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J Neurosci 27(11):2948–2957. doi:10.1523/JNEUROSCI.5289-06.2007 CrossRefPubMed

Barnes TD, Kubota Y, Hu D, Jin DZ, Graybiel AM (2005) Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437(7062):1158–1161CrossRefPubMed

Barnes SA, Sawiak SJ, Caprioli D, Jupp B, Buonincontri G, Mar AC, Harte MK, Fletcher PC, Robbins TW, Neill JC, Dalley JW (2014) Impaired limbic cortico-striatal structure and sustained visual attention in a rodent model of schizophrenia. Int J Neuropsychopharmacol. doi:10.1093/ijnp/pyu010 PubMedPubMedCentral

Belujon P, Patton MH, Grace AA (2014) Role of the prefrontal cortex in altered hippocampal-accumbens synaptic plasticity in a developmental animal model of schizophrenia. Cereb Cortex 24(4):968–977. doi:10.1093/cercor/bhs380 CrossRefPubMed

Bolding MS, White DM, Hadley JA, Weiler M, Holcomb HH, Lahti AC (2012) Antipsychotic drugs alter functional connectivity between the medial frontal cortex, hippocampus, and nucleus accumbens as measured by H215O PET. Front Psychiatry 3:105. doi:10.3389/fpsyt.2012.00105 PubMedPubMedCentral

Brody CD (1999) Correlations without synchrony. Neural Comput 11(7):1537–1551CrossRefPubMed

Bruno RM, Simons DJ (2002) Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 22(24):10966–10975 PubMed

Cao Y, Maran SK, Dhamala M, Jaeger D, Heck DH (2012) Behavior-related pauses in simple-spike activity of mouse Purkinje cells are linked to spike rate modulation. J Neurosci 32(25):8678–8685. doi:10.1523/JNEUROSCI.4969-11.2012 CrossRefPubMedPubMedCentral

Castane A, Santana N, Artigas F (2015) PCP-based mice models of schizophrenia: differential behavioral, neurochemical and cellular effects of acute and subchronic treatments. Psychopharmacology (Berl). doi:10.1007/s00213-015-3946-6

Chudasama Y, Bussey TJ, Muir JL (2001) Effects of selective thalamic and prelimbic cortex lesions on two types of visual discrimination and reversal learning. Eur J Neurosci 14(6):1009–1020 CrossRefPubMed

Cosgrove J, Newell TG (1991) Recovery of neuropsychological functions during reduction in use of phencyclidine. J Clin Psychol 47(1):159–169CrossRefPubMed

Coutureau E, Killcross S (2003) Inactivation of the infralimbic prefrontal cortex reinstates goal-directed responding in overtrained rats. Behav Brain Res 146(1–2):167–174CrossRefPubMed

Cullen TJ, Walker MA, Eastwood SL, Esiri MM, Harrison PJ, Crow TJ (2006) Anomalies of asymmetry of pyramidal cell density and structure in dorsolateral prefrontal cortex in schizophrenia. Br J Psychiatry 188:26–31CrossRefPubMed

Del Arco A, Mora F (2008) Prefrontal cortex-nucleus accumbens interaction: in vivo modulation by dopamine and glutamate in the prefrontal cortex. Pharmacol Biochem Behav 90(2):226–235. doi:10.1016/j.pbb.2008.04.011 CrossRefPubMed

Estrada-Sanchez AM, Burroughs CL, Cavaliere S, Barton SJ, Chen S, Yang XW, Rebec GV (2015) Cortical efferents lacking mutant huntingtin improve striatal neuronal activity and behavior in a conditional mouse model of Huntington’s disease. J Neurosci 35(10):4440–4451. doi:10.1523/JNEUROSCI.2812-14.2015 CrossRefPubMedPubMedCentral

Forbes D, Culum I, Lischka AR, Morgan DG, Peacock S, Forbes J, Forbes S (2009) Light therapy for managing cognitive, sleep, functional, behavioural, or psychiatric disturbances in dementia. Cochrane Database Syst Rev 4:CD003946doi:10.1002/14651858.CD003946.pub3

French SJ, Totterdell S (2003) Individual nucleus accumbens-projection neurons receive both basolateral amygdala and ventral subicular afferents in rats. Neuroscience 119(1):19–31CrossRefPubMed

Goda SA, Olszewski M, Piasecka J, Rejniak K, Whittington MA, Kasicki S, Hunt MJ (2015) Aberrant high frequency oscillations recorded in the rat nucleus accumbens in the methylazoxymethanol acetate neurodevelopmental model of schizophrenia. Prog Neuro-psychopharmacol Biol Psychiatry 61:44–51CrossRef

Gonzales KK, Smith Y (2015) Cholinergic interneurons in the dorsal and ventral striatum: anatomical and functional considerations in normal and diseased conditions. Ann N Y Acad Sci 1349(1):1–45. doi:10.1111/nyas.12762 CrossRefPubMedPubMedCentral

Goto Y, Grace AA (2005) Dopamine-dependent interactions between limbic and prefrontal cortical plasticity in the nucleus accumbens: disruption by cocaine sensitization. Neuron 47(2):255–266. doi:10.1016/j.neuron.2005.06.017 CrossRefPubMed

Grace AA (2000) Gating of information flow within the limbic system and the pathophysiology of schizophrenia. Brain Res Brain Res Rev 31(2–3):330–341CrossRefPubMed

Grayson B, Idris NF, Neill JC (2007) Atypical antipsychotics attenuate a sub-chronic PCP-induced cognitive deficit in the novel object recognition task in the rat. Behav Brain Res 184(1):31–38CrossRefPubMed

Grayson B, Leger M, Piercy C, Adamson L, Harte M, Neill JC (2015) Assessment of disease-related cognitive impairments using the novel object recognition (NOR) task in rodents. Behav Brain Res 285:176–193. doi:10.1016/j.bbr.2014.10.025 CrossRefPubMed

Green MF (1996) What are the functional consequences of neurocognitive deficits in schizophrenia? Am J Psychiatry 153(3):321–330. doi:10.1176/ajp.153.3.321 CrossRefPubMed

Halliday DM (2015) Nonparametric directionality measures for time series and point process data. J Integr Neurosci 14(2):253–277. doi:10.1142/S0219635215300127 CrossRefPubMed

Holt GR, Softky WR, Koch C, Douglas RJ (1996) Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75(5):1806–1814PubMed

Hradetzky E, Sanderson TM, Tsang TM, Sherwood JL, Fitzjohn SM, Lakics V, Malik N, Schoeffmann S, O'Neill MJ, Cheng TMK, Harris LW, Rahmoune H, Guest PC, Sher E, Collingridge GL, Holmes E, Tricklebank D, Bahn S (2012) The methylazoxymethanol acetate (MAM-E17) rat model: molecular and functional effects in the hippocampus. Neuropsychopharmacology 37(2):364–377. doi:10.1038/npp.2011.219 CrossRefPubMed

Ingallinesi M, Le Bouil L, Biguet NF, Do Thi A, la Cour CM, Millan MJ, Ravassard P, Mallet J, Meloni R (2014) Local inactivation of Gpr88 in the nucleus accumbens attenuates behavioral deficits elicited by the neonatal administration of phencyclidine in rats. Mol Psychiatry. doi:10.1038/mp.2014.92 PubMed

Javitt DC, Zukin SR (1991) Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148(10):1301–1308CrossRefPubMed

Jorgensen BP, Krych L, Pedersen TB, Plath N, Redrobe JP, Hansen AK, Nielsen DS, Pedersen C, Larsen C, Sorensen DB (2015) Investigating the long-term effect of subchronic phencyclidine-treatment on novel object recognition and the association between the gut microbiota and behavior in the animal model of schizophrenia. Physiol Behav 141:32–39. doi:10.1016/j.physbeh.2014.12.042 CrossRef

Kantrowitz JT, Javitt DC (2010) N-methyl-d-aspartate (NMDA) receptor dysfunction or dysregulation: the final common pathway on the road to schizophrenia? Brain Res Bull 83(3–4):108–121. doi:10.1016/j.brainresbull.2010.04.006 CrossRefPubMedPubMedCentral

Kargieman L, Santana N, Mengod G, Celada P, Artigas F (2007) Antipsychotic drugs reverse the disruption in prefrontal cortex function produced by NMDA receptor blockade with phencyclidine. Proc Natl Acad Sci USA 104(37):14843–14848CrossRefPubMedPubMedCentral

Kargieman L, Riga MS, Artigas F, Celada P (2012) Clozapine reverses phencyclidine-induced desynchronization of prefrontal cortex through a 5-HT(1A) receptor-dependent mechanism. Neuropsychopharmacology 37(3):723–733. doi:10.1038/npp.2011.249 CrossRefPubMed

Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13(4):400–408CrossRefPubMed

Krystal JH, Karper LP, Seibyl JP, Freeman GK, Delaney R, Bremner JD, Heninger GR, Bowers MB, Charney DS (1994) Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 51(3):199–214CrossRefPubMed

Leeson VC, Robbins TW, Franklin C, Harrison M, Harrison I, Ron MA, Barnes TRE, Joyce EM (2009) Dissociation of long-term verbal memory and fronto-executive impairment in first-episode psychosis. Psychol Med 39(11):1799–1808. doi:10.1017/S0033291709005935 CrossRefPubMed

Lodge DJ, Grace AA (2007) Aberrant hippocampal activity underlies the dopamine dysregulation in an animal model of schizophrenia. J Neurosci 27(42):11424–11430. doi:10.1523/JNEUROSCI.2847-07.2007 CrossRefPubMed

Mandillo S, Rinaldi A, Oliverio A, Mele A (2003) Repeated administration of phencyclidine, amphetamine and MK-801 selectively impairs spatial learning in mice: a possible model of psychotomimetic drug-induced cognitive deficits. Behav Pharmacol 14(7):533–544. doi:10.1097/01.fbp.0000095714.39553.56 CrossRefPubMed

Martinez ZA, Ellison GD, Geyer MA, Swerdlow NR (1999) Effects of sustained phencyclidine exposure on sensorimotor gating of startle in rats. Neuropsychopharmacology 21(1):28–39CrossRefPubMed

McNally JM, McCarley RW, Brown RE (2013) Impaired GABAergic neurotransmission in schizophrenia underlies impairments in cortical gamma band oscillations. Curr Psychiatry Rep. doi:10.1007/s11920-012-0346-z PubMedPubMedCentral

Miyauchi M, Neugebauer NM, Oyamada Y, Meltzer HY (2016) Nicotinic receptors and lurasidone-mediated reversal of phencyclidine-induced deficit in novel object recognition. Behav Brain Res 301:204–212. doi:10.1016/j.bbr.2015.10.044 CrossRefPubMed

Nuechterlein KH, Green MF, Kern RS, Baade LE, Barch DM, Cohen JD, Essock S, Fenton WS, Frese FJ 3rd, Gold JM, Goldberg T, Heaton RK, Keefe RS, Kraemer, H, Mesholam-Gately R, Seidman LJ, Stover E, Weinberger DR, Young AS, Zalcman S, Marder SR (2008) The MATRICS Consensus Cognitive Battery, part 1: test selection, reliability, and validity. Am J Psychiatry 165(2):203–213. doi:10.1176/appi.ajp.2007.07010042 CrossRefPubMed

Nuechterlein KH, Luck SJ, Lustig C, Sarter M (2009) CNTRICS final task selection: control of attention. Schizophr Bull 35(1):182–196. doi:10.1093/schbul/sbn158 CrossRefPubMedPubMedCentral

O’Donnell P, Greene J, Pabello N, Lewis BL, Grace AA (1999) Modulation of cell firing in the nucleus accumbens. Ann N Y Acad Sci 877:157–175CrossRefPubMed

Olney JW, Newcomer JW, Farber NB (1999) NMDA receptor hypofunction model of schizophrenia. J Psychiatr Res 33(6):523–533. doi:10.1016/S0022-3956(99)00029-1 CrossRefPubMed

Parkinson JA, Willoughby PJ, Robbins TW, Everitt BJ (2000) Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical-ventral striatopallidal systems. Behav Neurosci 114(1):42–63CrossRefPubMed

Paxinos G, Watson C (1986) The rat in stereotaxic coordinates. Academic Press, San Diego

Pezze MA, Dalley JW, Robbins TW (2009) Remediation of attentional dysfunction in rats with lesions of the medial prefrontal cortex by intra-accumbens administration of the dopamine D(2/3) receptor antagonist sulpiride. Psychopharmacology (Berl) 202(1–3):307–313. doi:10.1007/s00213-008-1384-4 CrossRef

Piyabhan P, Wetchateng T, Sireeratawong S (2013) Cognitive enhancement effects of Bacopa monnieri (Brahmi) on novel object recognition and NMDA receptor immunodensity in the prefrontal cortex and hippocampus of sub-chronic phencyclidine rat model of schizophrenia. J Med Assoc Thail 96(2):231–238

Quiroga QR, Kreuz T, Grassberger P (2002) Event synchronization: a simple and fast method to measure synchronicity and time delay patterns. Phys Rev E 66(4 Pt 1):041904CrossRef

Quiroga RQ, Nadasdy Z, Ben-Shaul Y (2004) Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16(8):1661–1687. doi:10.1162/089976604774201631 CrossRefPubMed

Rajagopal L, Massey BW, Huang M, Oyamada Y, Meltzer HY (2014) The novel object recognition test in rodents in relation to cognitive impairment in schizophrenia. Curr Pharm Des 20(31):5104–5114CrossRefPubMed

Rey HG, Pedreira C, Quiroga RQ (2015) Past, present and future of spike sorting techniques. Brain Res Bull 119(Pt B):106–117. doi:10.1016/j.brainresbull.2015.04.007 CrossRefPubMedPubMedCentral

Richter A, Petrovic A, Diekhof EK, Trost S, Wolter S, Gruber O (2015) Hyperresponsivity and impaired prefrontal control of the mesolimbic reward system in schizophrenia. J Psychiatr Res 71:8–15. doi:10.1016/j.jpsychires.2015.09.005 CrossRefPubMed

Riedel WJ, Mehta MA, Unema PJ (2006) Human cognition assessment in drug research. Curr Pharm Des 12(20):2525–2539CrossRefPubMed

Rosemann M, Ivashkevich A, Favor J, Dalke C, Holter SM, Becker L, Racz I, Bolle I, Klempt M, Rathkolb B, Kalaydjiev S, Adler T, Aguilar A, Hans W, Horsch M, Rozman J, Calzada-Wack J, Kunder S, Naton B, Gailus-Durner V, Fuchs H, Schultz H, Beckers J, Busch DH, Burbach JPH, Smidt MP, Quintanilla-Martinez L, Esposito I, Klopstock T, Klingenspor M, Ollert M, Wolf E, Wurst W, Zimmer A, de Angelis MH, Atkinson M, Heinzman U, Graw J (2010) Microphthalmia, parkinsonism, and enhanced nociception in Pitx3 (416insG) mice. Mamm Genome 21(1–2):13–27. doi:10.1007/s00335-009-9235-0 CrossRefPubMed

Rossi AF, Pessoa L, Desimone R, Ungerleider LG (2009) The prefrontal cortex and the executive control of attention. Exp Brain Res 192(3):489–497. doi:10.1007/s00221-008-1642-z CrossRefPubMed

Sahin C, Doostdar N, Neill JC (2016) Towards the development of improved tests for negative symptoms of schizophrenia in a validated animal model. Behav Brain Res 312:93–101CrossRefPubMed

Sharott A, Moll CK, Engler G, Denker M, Grun S, Engel AK (2009) Different subtypes of striatal neurons are selectively modulated by cortical oscillations. J Neurosci 29(14):4571–4585. doi:10.1523/JNEUROSCI.5097-08.2009 CrossRefPubMed

Shilliam CS, Dawson LA (2005) The effect of clozapine on extracellular dopamine levels in the shell subregion of the rat nucleus accumbens is reversed following chronic administration: comparison with a selective 5-HT(2C) receptor antagonist. Neuropsychopharmacology 30(2):372–380CrossRefPubMed

Snigdha S, Neill JC, McLean SL, Shemar GK, Cruise L, Shahid M, Henry B (2011) Phencyclidine (PCP)-induced disruption in cognitive performance is gender-specific and associated with a reduction in brain-derived neurotrophic factor (BDNF) in specific regions of the female rat brain. J Mol Neurosci 43(3):337–345. doi:10.1007/s12031-010-9447-5 CrossRefPubMed

Sofuoglu M, Mooney M (2009) Cholinergic functioning in stimulant addiction: implications for medications development. CNS Drugs 23(11):939–952. doi:10.2165/11310920-000000000-00000 CrossRefPubMedPubMedCentral

Sood P, Idris NF, Cole S, Grayson B, Neill JC, Young AM (2011) PD168077, a D(4) receptor agonist, reverses object recognition deficits in rats: potential role for D(4) receptor mechanisms in improving cognitive dysfunction in schizophrenia. J Psychopharmacol 25(6):792–800. doi:10.1177/0269881110387840 CrossRefPubMed

Stanford JA, Gerhardt GA (2001) Age-related changes in striatal function of freely-moving F344 rats. Neurobiol Aging 22(4):659–669CrossRefPubMed

Stern EA, Kincaid AE, Wilson CJ (1997) Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77(4):1697–1715PubMed

Sutcliffe JS, Marshall KM, Neill JC (2007) Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behav Brain Res 177(1):117–125CrossRefPubMed

Sutcliffe JS, Rhaman F, Marshall KM, Neill JC (2008) Oestradiol attenuates the cognitive deficit induced by acute phencyclidine treatment in mature female hooded-Lister rats. J Psychopharmacol 22(8):918–922. doi:10.1177/0269881107083839 CrossRefPubMed

Uhlhaas PJ, Singer W (2010) Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11(2):100–113CrossRefPubMed

van Erp TG, Hibar DP, Rasmussen JM, Glahn DC, Pearlson GD, Andreassen OA, Agartz I, Westlye LT, Hauvik UK, Dale AM, Melle I, Hartberg CB, Gruber O, Kraemer B, Zilles D, Donohue G, Kelly S, McDonald C, Morris DW, Cannon DM, Corbin A, Machielsen MW, Koenders L, de Haan L, Veltman DJ, Satterthwaite TD, Wolf DH, Gur RC, Gur RE, Potkin SG, Mathalon DH, Mueller BA, Preda A, Macciardi F, Ehrlich S, Walton E, Hass J, Calhoun VD, Bockholt HJ, Sponheim SR, Shoemaker JM, van Haren NE, Pol HE, Ophoff RA, Kahn RS, Roiz-Santianez R, Crespo-Facorro B, Wang L, Alpert KI, Jonsson EG, Dimitrova R, Bois C, Whalley HC, Mcintosh AM, Lawrie SM, Hashimoto R, Thompson PM, Turner JA (2015) Subcortical brain volume abnormalities in 2028 individuals with schizophrenia and 2540 healthy controls via the ENIGMA consortium. Mol Psychiatry. doi:10.1038/mp.2015.118

Weible AP, Rowland DC, Pang R, Kentros C (2009) Neural correlates of novel object and novel location recognition behavior in the mouse anterior cingulate cortex. J Neurophysiol 102(4):2055–2068. doi:10.1152/jn.00214.2009 CrossRefPubMed

Woo TU, Spencer K, McCarley RW (2010) Gamma oscillation deficits and the onset and early progression of schizophrenia. Harv Rev Psychiatry 18(3):173–189. doi:10.3109/10673221003747609 CrossRefPubMedPubMedCentral

Wood DA, Rebec GV (2004) Dissociation of core and shell single-unit activity in the nucleus accumbens in free-choice novelty. Behav Brain Res 152(1):59–66. doi:10.1016/j.bbr.2003.09.038 PubMed

Yoon T, Okada J, Jung MW, Kim JJ (2008) Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learn Mem 15(3):97–105. doi:10.1101/lm.850808 CrossRefPubMedPubMedCentral

Young AM, Stubbendorff C, Valencia M, Gerdjikov TV (2015) Disruption of medial prefrontal synchrony in the subchronic phencyclidine model of schizophrenia in rats. Neuroscience 287:157–163. doi:10.1016/j.neuroscience.2014.12.014 CrossRefPubMedPubMedCentral

Title: Altered cortico-striatal crosstalk underlies object recognition memory deficits in the sub-chronic phencyclidine model of schizophrenia
Authors: Aman Asif-Malik
Daniel Dautan
Andrew M. J. Young
Todor V. Gerdjikov
Publication date: 01-09-2017
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 7/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-017-1393-3

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Altered cortico-striatal crosstalk underlies object recognition memory deficits in the sub-chronic phencyclidine model of schizophrenia

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 7/2017

Top-down cortical interactions in visuospatial attention

Homeostatic regulation through GABA and acetylcholine muscarinic receptors of motor trigeminal neurons following sleep deprivation

Erratum to: Interhemispheric gene expression differences in the cerebral cortex of humans and macaque monkeys

Neural pathways subserving face-based mentalizing

Quantification of neuronal density across cortical depth using automated 3D analysis of confocal image stacks

Interhemispheric gene expression differences in the cerebral cortex of humans and macaque monkeys