Skip to main content
SpringerLink
Log in

Morphological, structural, and functional alterations of the prefrontal cortex and the basolateral amygdala after early lesion of the rat mediodorsal thalamus

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

Early postnatal damage to the mediodorsal thalamus (MD) produces deficits in cognition and behavior believed to be associated with early prefrontal cortical maldevelopment. We assessed the role of MD afferents during development on the morphological and functional maturation of the prefrontal cortex (PFC) and the basolateral amygdala (BLA). Sprague—Dawley rat pups (n = 56) received a bilateral electrolytic lesion of the MD or a MD Sham lesion on postnatal day 4. 7 weeks later, all rats were tested in anxiety-related and cognitive paradigms using the elevated plus maze and novel object recognition tests. Following behavioral testing (P70), rats were killed and the baseline expression of C-Fos protein and the number of GABAergic neurons were evaluated in the PFC and the BLA. The dendritic morphology and spine density in the PFC using Golgi-Cox staining was also evaluated. Adult rats with early postnatal bilateral MD damage exhibited disrupted recognition memory and increased anxiety-like behaviors. The lesion also caused a significant diminution of C-Fos immunolabeling and an increase of the number of GABAergic neurons in the PFC. In the BLA, the number of GABAergic neurons was significantly reduced, associated with an increase in C-Fos immunolabeling. Furthermore, in the PFC the lesion induced a significant reduction in dendritic branching and spine density. Our data are consistent with the hypothesis that the MD plays a role in the development of the PFC and, therefore, may be a good animal model to investigate cognitive symptoms associated with schizophrenia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Abercrombie M, Johnson ML (1946) Quantitative histology of Wallerian degeneration I. Nuclear population in rabbit sciatic nerve. J Anat Lond 80:37–50

    Google Scholar 

  • Akbarian S, Kim JJ, Potkin SG, Hagman JO, Tafazzoli A, Bunney WE, Jones EG (1995) Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry 52:258–266

    Article  CAS  PubMed  Google Scholar 

  • Alcantara S, Ferrer I, Soriano E (1993) Postnatal development of parvalbumin and calbindin D28K immunoreactivities in the cerebral cortex of the rat. Anat Embryol (Berl.) 188: 63–73

    Article  CAS  Google Scholar 

  • Altman J, Bayer SA (1995) Atlas of prenatal rat brain development. CRC, Boca Raton

    Google Scholar 

  • Armstrong E, Parker B (1986) A new Golgi method for adult human brains. J Neurosci Methods 17:247–254

    Article  CAS  PubMed  Google Scholar 

  • Barker GRI, 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 27:2948–2957

    Article  CAS  PubMed  Google Scholar 

  • Benes FM (1989) Myelination of cortical-hippocampal relays during late adolescence. Schizophr Bull 15:585–593

    Article  CAS  PubMed  Google Scholar 

  • Berdel B, Morys J (2000) Expression of calbindin-D28k and parvalbumin during development of rat’s basolateral amygdaloid complex. Int J Dev Neurosci 18:501–513

    Article  CAS  PubMed  Google Scholar 

  • Berendse HW, Galis de Graaf Y, Groenewegen HJ (1992) Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol 316:314–347

    Article  CAS  PubMed  Google Scholar 

  • Berry M (1974) Development of the cerebral neocortex of the rat; in Gottlieb G (ed): Aspects of Neurogenesis. Academic Press, New York, 2:7–67

    Google Scholar 

  • Bishop S, Duncan J, Brett M, Lawrence AD (2004) Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli. Nat Neurosci 7:184–188

    Article  CAS  PubMed  Google Scholar 

  • Bouwmeester H, Wolterink G, van Ree JM (2002) Neonatal development of projections from the basolateral amygdala to prefrontal, striatal, and thalamic structures in the rat. J Comp Neurol 442:239–249

    Article  PubMed  Google Scholar 

  • Broadbelt K, Byne WB, Jones LB (2002) Evidence for a decrease in primary and secondary basilar dendrites on pyramidal cells in area 32 of schizophrenic prefrontal cortex. Schizophr Res 58:75–81

    Article  PubMed  Google Scholar 

  • Brummelte S, Neddens J, Teuchert-Noodt G (2007) Alteration in the GABAergic network of the prefrontal cortex in a potential animal model of psychosis. J Neural Transm 114(5):539–547

    Article  CAS  PubMed  Google Scholar 

  • Callaway JC, Lasser-Ross N, Ross WN (1995) IPSPs strongly inhibit climbing fiber-activated [Ca 2+]i increases in the dendrites of cerebellar Purkinje neurons. J Neurosci 15:2777–2787

    CAS  PubMed  Google Scholar 

  • Cassell MD, Chittick CA, Siegel MA, Wright DJ (1989) Collateralization of the amygdaloid projections of the rat prelimbic and infralimbic cortices. J Comp Neurol 279:235–248

    Article  CAS  PubMed  Google Scholar 

  • Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375–475

    Article  CAS  PubMed  Google Scholar 

  • Chauveau F, Celerier A, Ognard R, Pierard C, Beracochea D (2005) Effects of ibotenic acid lesions of the mediodorsal thalamus on memory: relationship with emotional processes in mice. Behav Brain Res 156:215–223

    Article  CAS  PubMed  Google Scholar 

  • Chiba T, Kayahara T, Nakano K (2001) Efferent projections of infralimbic and prelimbic areas of the medial prefrontal cortex in the Japanese monkey, Macaca fuscata. Brain Res 888:83–101

    Article  CAS  PubMed  Google Scholar 

  • Chronwall B, Wolff JR (1980) Prenatal and postnatal development of GABA accumulating cells in the occipital neocortex of rat. J Comp Neurol 190:187–208

    Article  CAS  PubMed  Google Scholar 

  • Cohen S, Greenberg ME (2008) Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu. Rev Cell. Dev Biol 24:183–209

    CAS  Google Scholar 

  • Cotman CW, Nieto-Sampedro M (1984) Cell biology of synaptic plasticity. Science 225:1287–1294

    Article  CAS  PubMed  Google Scholar 

  • Cross L, Brown MW, Aggleton JP, Warburton EC (2012) The medial dorsal thalamic nucleus and the medial prefrontal cortex of the rat function together to support associative recognition and recency but not item recognition. Learn Mem 20:41–50

    Article  PubMed  Google Scholar 

  • Curran T, Morgan JI (1986) Barium modulates c-fos expression and post-translational modification. Proc Natl Acad Sci USA 83:8521–8524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dammasch IE, Wagner GP, Wolff JR (1986) Self-stabilization of neuronal networks. I. The compensation algorithm for synaptogenesis. Biol Cybern 54(4–5):211–222

    Article  CAS  PubMed  Google Scholar 

  • Davis M, Rainnie D, Cassell M (1994) Neurotransmission in the rat amygdala related to fear and anxiety. Trends Neurosci 17:208–214

    Article  CAS  PubMed  Google Scholar 

  • Dawirs RR, Teuchert-Noodt G, Czaniera R (1993a) Maturation of the dopamine innervation during postnatal development of the prefrontal cortex in gerbils (Meriones unguiculatus). A quantitative immunocytochemical study. J Hirnforsch 34:281–290

  • Dawirs RR, Teuchert-Noodt G, Molthagen M (1993b) Indication of methamphetamine-induced reactive synaptogenesis in the prefrontal cortex of gerbils Meriones unguiculatus. Eur J Pharmacol 421:89–97

  • Del Rio JA, Soriano E, Ferrer I (1992) Development of GABA-immunoreactivity in the neocortex of the mouse. J Comp Neurol 326:501–526

    Article  CAS  PubMed  Google Scholar 

  • Ennaceur A, Aggleton JP (1994) Spontaneous recognition of object configurations in rats: effects of fornix lesions. Exp Brain Res 100(1):85–92

    Article  CAS  PubMed  Google Scholar 

  • Etkin A, Wager TD (2007) Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry 164:1476–1488

    Article  PubMed Central  PubMed  Google Scholar 

  • Fahy FL, Riches IP, Brown MW (1993) Neuronal signals of importance to the performance of visual recognition memory tasks: Evidence from recordings of single neurons in the medial thalamus of primates. Progr Brain Res 95:401–416

    Article  CAS  Google Scholar 

  • File SE, Gonzalez LE, Gallant R (1998) Role of the basolateral nucleus of the amygdala in the formation of a phobia. Neuropsychopharmacology 19:397–405

    Article  CAS  PubMed  Google Scholar 

  • Flores G, Alquicer G, Silva-Gomez AB, Zaldivar G, Stewart J, Quirion R, Srivastava LK (2005) Alterations in dendritic morphology of prefrontal cortical and nucleus accumbens neurons in post-pubertal rats after neonatal excitotoxic lesions of the ventral hippocampus. Neuroscience 133:463–470

    Article  CAS  PubMed  Google Scholar 

  • Floresco SB, Braaksma DN, Phillips AG (1999) Thalamic–cortical–striatal circuitry subserves working memory during delayed responding on a radial arm maze. J Neurosci 19:11061–11071

    CAS  PubMed  Google Scholar 

  • Gabbott PL, Warner TA, Jays PR, Bacon SJ (2003) Areal and synaptic interconnectivity of prelimbic (area 32), infralimbic (area 25) and insular cortices in the rat. Brain Res 993:59–71

    Article  CAS  PubMed  Google Scholar 

  • Garey LJ, Ong WY, Patel TS et al (1998) Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J Neurol Neurosurg Psychiatry 65:446–453

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ghashghaei HT, Barbas H (2002) Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 115(1261):1279

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gillessen T, Alzheimer C (1997) Amplification of EPSPs by low Ni 2 + and amiloride-sensitive Ca 2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Neurosci 77:1639–1643

    CAS  Google Scholar 

  • Glantz LA, Lewis DA (2000) Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 57:65–67

    Article  CAS  PubMed  Google Scholar 

  • Goldman-Rakic PS, Porrino LJ (1985) The primate mediodorsal (MD) nucleus and its projection to the frontal lobe. J Comp Neurol 242:535–560

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Burgos G, Lewis DA (2008) NMDA receptor hypofunction, parvalbumin-positive neurons, and cortical gamma oscillations in schizophrenia. Schizophr Bull 38:950–957

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Guldin WO, Pritzel M, Markowitsch HJ (1981) Prefrontal cortex of the mouse defined as cortical projection area of the thalamic mediodorsal nucleus. Brain Behav Evol 19:93–107

    Article  CAS  PubMed  Google Scholar 

  • Handley SL, McBlane JW (1993) An assessment of the elevated plus-maze for studying anxiety and anxiety-modulating drugs. J Pharmacol Toxicol Methods 29:129–138

    Article  CAS  PubMed  Google Scholar 

  • Handley SL, Mithani S (1984) Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of ‘fear’-motivated behavior. Naunyn Schmiedebergs Arch Pharmacol 327:1–5

    Article  CAS  PubMed  Google Scholar 

  • Herrera DG, Robertson HA (1996) Activation of c-fos in the brain. Prog Neurobiol 50:83–107

    Article  CAS  PubMed  Google Scholar 

  • Howard MW, Rizzuto DS, Caplan JB, Madsen JR, Lisman J, Aschenbrenner-Scheibe R, Schulze-Bonhage A, Kahana MJ (2003) Gamma oscillations correlate with working memory load in humans. Cereb Cortex 13:1369–1374

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Hurley KM, Herbert H, Moga MM, Saper CB (1991) Efferent projections of the infralimbic cortex of the rat. J Comp Neurol 308:249–276

    Article  CAS  PubMed  Google Scholar 

  • Isseroff A, Rosvold HE, Galkin TW, Goldman-Rakic PS (1982) Spatial memory impairments following damage to the mediodorsal nucleus of the thalamus in rhesus monkeys. Brain Res 232:97–113

    Article  CAS  PubMed  Google Scholar 

  • Jones L, Johnson N, Byne W (2002) Alterations in MAP2 staining in area 9 and 32 of schizophrenic prefrontal cortex. Psychiatry Res 114:137–148

    Article  CAS  PubMed  Google Scholar 

  • Kesner RP, Hunt ME, Williams JM, Long JM (1996) Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cereb Cortex 6:311–318

    Article  CAS  PubMed  Google Scholar 

  • Kolb B, Buhrmann K, McDonald R, Sutherland RJ (1994) Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. Cereb Cortex 4:664–680

    Article  CAS  PubMed  Google Scholar 

  • Kosaka H, Omori M, Murata T, Iidaka T, Yamada H, Okada T, Takahashi T, Sadato N, Itoh H, Yonekura Y, Wada Y (2002) Differential amygdala response during facial recognition in patients with schizophrenia: an fMRI study. Schizophr Res 57:87–95

    Article  CAS  PubMed  Google Scholar 

  • Krettek JE, Price JL (1977) The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171:157–192

    Article  CAS  PubMed  Google Scholar 

  • Kuroda M, Murakami K, Kishi K, Price JL (1995) Thalamocortical synapses between axons from the mediodorsal thalamic nucleus and pyramidal cells in the prelimbic cortex of the rat. J Comp Neurol 356:143–151

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Labiner DM, Butler LS, Cao Z, Hosford DA, Shin C, McNamara JO (1993) Induction of c-fos mRNA by kindled seizures: complex relationship with neuronal burst firing. J Neurosci 13:744–751

    CAS  PubMed  Google Scholar 

  • Lacroix L, Broersen LM, Weiner I, Feldon J (1998) The effects of excitotoxic lesion of the medial prefrontal cortex on latent inhibition, prepulse inhibition, food hoarding, elevated plus maze, active avoidance and locomotor activity in the rat. Neuroscience 84:431–442

    Article  CAS  PubMed  Google Scholar 

  • Lapiz-Bluhm MD, Bondi CO, Doyen J, Rodriguez GA, Bedard-Arana T, Morilak DA (2008) Behavioral assays to model cognitive and affective dimensions of depression and anxiety in rats. J Neuroendocrinol 20:1115–1137

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • LeDoux J (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23:727–738

    Article  PubMed  Google Scholar 

  • Leonard CM (1969) The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. Brain Res 12(2):321–343

    Article  CAS  PubMed  Google Scholar 

  • Li CR, Huang GB, Sui ZY, Han EH, Chung YC (2010) Effects of 6-hydroxydopamine lesioning of the medial prefrontal cortex on social interactions in adolescent and adult rats. Brain Res 1346:183–189

    Article  CAS  PubMed  Google Scholar 

  • Lipska BK, Weinberger DR (1993) Delayed effects of neonatal hippocampal damage on haloperidol induced catalepsy and apomorphine-induced stereotypic behaviours in the rat. Dev Brain Res 75:213–222

    Article  CAS  Google Scholar 

  • Maaswinkel H, Gispen WH, Spruijt BM (1996) Effects of an electrolytic lesion of the prelimbic area on anxiety-related and cognitive tasks in the rat. Behav Brain Res 79:51–59

    Article  CAS  PubMed  Google Scholar 

  • Marmolejo N, Paez J, Levitt JB, Jones LB (2012) Early postnatal lesion of the medial dorsal nucleus leads to loss of dendrites and spines in adult prefrontal cortex. Dev Neurosci 34(6):463–476

    Article  CAS  PubMed  Google Scholar 

  • Marmolejo N, Paez J, Levitt JB, Jones LB (2013) Early postnatal lesion of the medialdorsal nucleus leads to loss of dendrites and spines in adult prefrontal cortex. Dev Neurosci 34:463–476

    Article  PubMed Central  CAS  Google Scholar 

  • McAllister AK (2000) Cellular and molecular mechanisms of dendrite growth. Cereb Cortex 10(10):963–973

    Article  CAS  PubMed  Google Scholar 

  • McAlonan GM, Robbins TW, Everitt BJ (1993) Effects of medial dorsal thalamic and ventral pallidal lesions on the acquisition of a conditioned place preference: further evidence for the involvement of the ventral striatopallidal system in reward-related processes. Neuroscience 52:605–620

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ (1991) Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44:1–14

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Progr Neurobiol 55:257–332

    Article  CAS  Google Scholar 

  • McDonald AJ, Mascagni F (2001) Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105:681–693

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ, Mascagni F, Guo L (1996) Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 71:55–75

    Article  CAS  PubMed  Google Scholar 

  • Mitchell AS, Dalrymple Alford JC (2005) Dissociable memory effects after medial thalamus lesions in the rat. Eur J Neurosci 22:973–985

    Article  PubMed  Google Scholar 

  • Mitchell AS, Browning PGF, 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moreira CM, Masson S, Carvalho MC, Brandao ML (2007) Exploratory behaviour of rats in the elevated plus maze is differentially sensitive to inactivation of the basolateral and central amygdaloid nuclei. Brain Res Bull 71:466–474

    Article  PubMed  Google Scholar 

  • Negyessy L, Hámori J, Bentivoglio M (1998) Contralateral cortical projection to the mediodorsal thalamic nucleus: origin and synaptic organization in the rat. Neuroscience 84:741–753

    Article  CAS  PubMed  Google Scholar 

  • Ottersen OP, Ben-Ari Y (1979) Afferent connections to the amygdaloid complex of the rat and cat. J Comp Neurol 187:401–424

    Article  CAS  PubMed  Google Scholar 

  • Ouhaz Z, Ba-M’hame S, Mitchell AS, Elidrissi A, Bennis M (2015) Behavioral and cognitive changes after early postnatal lesions of the rat mediodorsal thalamus. Behav Brain Res 292:219–232

    Article  PubMed Central  PubMed  Google Scholar 

  • Parker A, Eacott MJ, Gaffan D (1997) The recognition memory deficit caused by mediodorsal thalamic lesion in non-human primates: A comparison with rhinal cortex lesion. Eur J Neurosci 9:2423–2431

    Article  CAS  PubMed  Google Scholar 

  • Parnaudeau S, O’Neill PK, Bolkan SS, Ward RD, Abbas AI, Roth BL, Balsam PD, Gordon JA, Kellendonk C (2013) Inhibition of mediodorsal thalamus disrupts thalamofrontal connectivity and cognition. Neuron 77:1151–1162

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Parnaudeau S, Taylor K, Bolkan SS, Ward RD, Balsam PD, Kellendonk C (2015) Mediodorsal thalamus hypofunction impairs flexible goal-directed behavior. Biol Psychiatry 77:445–453

    Article  PubMed  Google Scholar 

  • Paxinos G, Watson C (2008) The rat brain: in stereotaxic coordinates, vol 6. Elsevier Academic Press, San Diego

    Google Scholar 

  • Pesold C, Treit D (1995) The central and basolateral amygdala differentially mediate the anxiolytic effects of benzodiazepines. Brain Res 671:213–221

    Article  CAS  PubMed  Google Scholar 

  • Phelps EA, Le Doux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175–187

    Article  CAS  PubMed  Google Scholar 

  • Phifer CB, Terry LM (1986) Use of hypothermia for general anesthesia in preweanling rodents. Physiol Behav 38:887–890

    Article  CAS  PubMed  Google Scholar 

  • Prager EM, Pidoplichko VI, Aroniadou-Anderjaska V, Apland JP, Braga MF (2014) Pathophysiological mechanisms underlying increased anxiety after soman exposure: reduced GABAergic inhibition in the basolateral amygdala. Neurotoxicology 44:335–343

    Article  CAS  PubMed  Google Scholar 

  • Quirk GJ, Beer JS (2006) Prefrontal involvement in the regulation of emotion: convergence of rat and human studies. Curr Opin Neurobiol 16:723–727

    Article  CAS  PubMed  Google Scholar 

  • Ragozzino M, Detrick S, Kesner R (2002) The effects of prelimbic and infralimbic lesions on working memory for visual objects in rats. Neurobiol Learn Mem 77:29–43

    Article  PubMed  Google Scholar 

  • Rajan I, Cline HT (1998) Glutamate receptor activity is required for normal development of tectal cell dendrites in vivo. J Neurosci 18:7836–7846

    CAS  PubMed  Google Scholar 

  • Rauch SL, Shin LM, Phelps EA (2006) Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research – past, present, and future. Biol Psychiatry 60:376–382

    Article  PubMed  Google Scholar 

  • Rauch AV, Reker M, Ohrmann P, Pedersen A, Bauer J, Dannlowski U, Harding L, Koelkebeck K, Konrad C, Kugel H, Arolt V, Heindel W, Suslow T (2010) Increased amygdala activation during automatic processing of facial emotion in schizophrenia. Psychiatry Res 182:200–206

    Article  PubMed  Google Scholar 

  • Rios O, Villalobos J (2004) Postnatal development of the afferent projections from the dorsomedial thalamic nucleus to the frontal cortex in mice. Dev Brain Res 150(1):47–50

    Article  CAS  PubMed  Google Scholar 

  • Room P, Russchen FT, Groenewegen HJ, Lohman AH (1985) Efferent connections of the prelimbic (area 32) and the infralimbic (area 25) cortices: An anterograde tracing study in the cat. J Comp Neurol 242:40–55

    Article  CAS  PubMed  Google Scholar 

  • Rose JE, Woolsey CN (1948) The orbitofrontal cortex and its connections with the mediodorsal nucleus in rabbit, sheep and cat. Res Publ Assoc Res Nerv Ment Dis 27(1):210–232

    PubMed  Google Scholar 

  • Sah P, Faber ESL, Lopez de Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83(3):803–834

    Article  CAS  PubMed  Google Scholar 

  • Sesack SR, Deutch AY, Roth RH, Bunney BS (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

    Article  CAS  PubMed  Google Scholar 

  • Sgambato V et al (1997) Effect of electrical stimulation of the cerebral cortex on the expression of the Fos protein in the basal ganglia. Neuroscience 81:93–112

    Article  CAS  PubMed  Google Scholar 

  • Sheng M, Greenberg ME (1990) The regulation and function of c-fos and other immediate early genes in the nervous system. Neuron 4:477–485

    Article  CAS  PubMed  Google Scholar 

  • Shinonaga Y, Takada M, Mizuno N (1994) Topographic organization of collateral projections from the basolateral amygdaloid nucleus to both the prefrontal cortex and nucleus accumbens in the rat. Neuroscience 58:389–397

    Article  CAS  PubMed  Google Scholar 

  • Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87(4):387–406

    CAS  PubMed Central  PubMed  Google Scholar 

  • Silva-Gomez AB, Rojas D, Juarez I, Flores G (2003) Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 983:128–136

    Article  CAS  PubMed  Google Scholar 

  • Souza A, Dussan-Sarria JA, Medeiros LF, Souza AC, Oliveira C, Scarabelot VL, Adachi LN, Winkelmann-Duarte EC, Philippi-Martins BB, Netto CA, Caumo W, Torres ILS (2014) Neonatal hypoxic–ischemic encephalopathy reduces c-Fos activation in the rat hippocampus: evidence of a long-lasting effect. Int J Dev Neurosci 38:213–222

    Article  CAS  PubMed  Google Scholar 

  • Su HS, Bentivoglio M (1990) Thalamic midline cell populations projecting to the nucleus accumbens, amygdala and hippocampus in the rat. J Comp Neurol 297:582–593

    Article  Google Scholar 

  • Thompson M, Weickert CS, Wyatt E, Webster MJ (2009) Decreased glutamic acid decarboxylase67 mRNA expression in multiple brain areas of patients with schizophrenia and mood disorders. J Psychiatr Res 43(11):970–977

    Article  PubMed  Google Scholar 

  • Thomases DR, Cass DK, Tseng KY (2013) Periadolescent exposure to the NMDA receptor antagonist MK-801 impairs the functional maturation of local GABAergic circuits in the adult prefrontal cortex. J Neurosci 33:26–34

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tseng KY, Chambers RA, Lipska BK (2009) The neonatal ventral hippocampal lesion as a heuristic neurodevelopmental model of schizophrenia. Behav Brain Res 204:295–305

    Article  PubMed  Google Scholar 

  • Uhlhaas PJ, Roux F, Singer W (2013) Thalamocortical synchronization and cognition: implications for schizophrenia? Neuron 77(6):997–999

    Article  CAS  PubMed  Google Scholar 

  • Uylings HB, Groenewegen HJ, Kolb B (2003) Do rats have a prefrontal cortex? Behav BrainRes 146:3–17

    Google Scholar 

  • Van Eden CG (1986) Development of connections between the mediodorsal nucleus of the thalamus and the prefrontal cortex in the rat. J Comp Neurol 244:349–359

    Article  PubMed  Google Scholar 

  • Van Eden CG, Uylings HB (1985) Postnatal volumetric development of the prefrontal cortex in the rat. J Comp Neurol 241:268–274

    Article  PubMed  Google Scholar 

  • Van Ooyen A, van Pelt J, Corner MA (1995) Implication of activity-dependent neurite outgrowth for neuronal morphology and network development. J Theor Biol 172:63–82

    Article  PubMed  Google Scholar 

  • Van Pelt J, van Ooyen A, Corner MA (1996) Growth cone dynamics and activity-dependent processes in neuronal network development. Prog Brain Res 108:333–346

    Article  PubMed  Google Scholar 

  • Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51(1):32–58

    Article  CAS  PubMed  Google Scholar 

  • Villarreal G, King CY (2001) Brain imaging in posttraumatic stress disorder. Semin Clin Neuropsychiatry 6:131–45

    Article  CAS  PubMed  Google Scholar 

  • Vincent SL, Pabreza L, Benes FM (1995) Postnatal maturation of GABA immunoreactive neurons of rat medial prefrontal cortex. J Comp Neurol 355:81–92

    Article  CAS  PubMed  Google Scholar 

  • Volk DW, Lewis DA (2003) Effects of a mediodorsal thalamus lesion on prefrontal inhibitory circuitry: implications for schizophrenia. Biol Psychiatry 53:385–389

    Article  PubMed  Google Scholar 

  • Volk DW, Austin MC, Pierri JN, Sampson AR, Lewis DA (2000) Decreased glutamic acid decarboxylase67 messenger RNA expression in a subset of prefrontal cortical gammaaminobutyric acid neurons in subjects with schizophrenia. Arch Gen Psychiatry 57:237–245

    Article  CAS  PubMed  Google Scholar 

  • Wise SP, Fleshman JW, Jones EG (1979) Maturation of pyramidal cell form in relation to developing afferent and efferent connections of the rat somatic sensory cortex. J Neurosci 4:1275–1297

    Article  CAS  Google Scholar 

  • Wolff JR, Wagner GP (1983) Self organization in synaptogenesis: interaction between the formation of excitatory and inhibitory synapses. In: Basar F, Flohr H, Haken H, Mandell AJ. (eds) Synergetics in the brain. Springer, Berlin, pp 50–59

    Chapter  Google Scholar 

  • Xing J, Ginty DD, Greenberg ME (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273:959–963

    Article  CAS  PubMed  Google Scholar 

  • Zola-Morgan S, Squire LR (1985) Amnesia in monkeys after lesions of the mediodorsal nucleus of the thalamus. Ann Neurol 17:558–564

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by NEUREN Project (PIRSES-GA-2012-318997). We thank Prof. Alessandro Vercelli (Calvalieri-Ottolenghi Foundation, Regione Gonzale 10, Orbassano, Torino, Italy) for his help in achieving Sholl analysis. We thank also Dr Howard M Cooper (INSERM 1208–Stem Cell and Brain Research Institute Head - Department of Chronobiology & Affective Disorders, Bron France) for reading and editing the manuscript.

Author information

Authors and Affiliations

  1. Lab of Pharmacology, Neurobiology and Behavior (URAC-37), Faculty of Sciences Semlalia, Cadi Ayyad University, 40000, Marrakech, Morocco

    Zakaria Ouhaz, Saadia Ba-M’hamed & Mohamed Bennis

Authors
  1. Zakaria Ouhaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saadia Ba-M’hamed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohamed Bennis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohamed Bennis.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ouhaz, Z., Ba-M’hamed, S. & Bennis, M. Morphological, structural, and functional alterations of the prefrontal cortex and the basolateral amygdala after early lesion of the rat mediodorsal thalamus. Brain Struct Funct 222, 2527–2545 (2017). https://doi.org/10.1007/s00429-016-1354-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-016-1354-2

Keywords

Search

Navigation