Publication Cover
Nutritional Neuroscience
An International Journal on Nutrition, Diet and Nervous System
Latest Articles
0
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Prenatal protein malnutrition decreases neuron numbers in the parahippocampal region but not prefrontal cortex in adult rats

, , , , , , , & show all

References

  • Rushmore RJ, McGaughy JA, Amaral AC, Mokler DJ, Morgane PJ, Galler JR, Rosene DL. The neural basis of attentional alterations in prenatally protein malnourished rats. Cereb Cortex. 2021;31(1):497–512.
  • Morgane P, Galler J, Mokler D. A review of systems and networks of the limbic forebrain/limbic midbrain. Prog Neurobiol. 2005;75(2):143–60.
  • Rushmore RJ, McGaughy JA, Mokler DJ, Rosene DL. The enduring effect of prenatal protein malnutrition on brain anatomy, physiology and behavior. Nutr Neurosci. 2020 Dec 14: 25(7):1–8.
  • Galler JR, Ramsey F, Solimano G, Lowell WE, Mason E. The influence of early malnutrition on subsequent behavioral development. I. Degree of impairment in intellectual performance. J Am Acad Child Psychiatry. 1983;22(1):8–15.
  • Galler JR, Bryce CP, Zichlin ML, Fitzmaurice G, Eaglesfield GD, Waber DP. Infant malnutrition is associated with persisting attention deficits in middle adulthood. J Nutr. 2012;142(4):788–94.
  • Waber DP, Bryce CP, Fitzmaurice GM, Zichlin ML, McGaughy J, Girard JM, Galler JR. Neuropsychological outcomes at midlife following moderate to severe malnutrition in infancy. Neuropsychology. 2014;28(4):530–40.
  • Tonkiss J, Galler JR. Prenatal protein malnutrition and working memory performance in adult rats. Behav Brain Res. 1990;40(2):95–107.
  • Morgane PJ, Austin-LaFrance R, Bronzino J, Tonkiss J, Díaz-Cintra S, Cintra L, et al. Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev. 1993;17(1):91–128.
  • Wolf C, Almli CR, Finger S, Ryan S, Morgane PJ. Behavioral effects of severe and moderate early malnutrition. Physiol Behav. 1986;38(5):725–30.
  • Almeida SS, Tonkiss J, Galler JR. Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test. Physiol Behav. 1996a;60(2):675–80.
  • Almeida SS, Tonkiss J, Galler JR. Prenatal protein malnutrition affects avoidance but not escape behavior in the elevated T-maze test. Physiol Behav. 1996b;60(1):191–5.
  • Tonkiss J, Galler JR, Formica RN, Shukitt-Hale B, Timm RR. Fetal protein malnutrition impairs acquisition of a DRL task in adult rats. Physiol Behav. 1990;48(1):73–7.
  • McGaughy JA, Amaral AC, Rushmore RJ, Mokler DJ, Morgane PJ, Rosene DL, Galler JR. Prenatal malnutrition leads to deficits in attentional set shifting and decreases metabolic activity in prefrontal subregions that control executive function. Dev Neurosci. 2014;36(6):532–41.
  • Amaral AC, Jakovcevski M, McGaughy JA, Calderwood SK, Mokler DJ, Rushmore RJ, et al. Prenatal protein malnutrition decreases KCNJ3 and 2DG activity in rat prefrontal cortex. Neuroscience. 2015;286:79–86.
  • Diáz-Cintra S, Cintra L, Galván A, Aguilar A, Kemper T, Morgane PJ. Effects of prenatal protein deprivation on postnatal development of granule cells in the fascia dentata. J Comp Neurol. 1991;310(3):356–64. doi:10.1002/cne.903100306.
  • Díaz-Cintra S, García-Ruiz M, Corkidi G, Cintra L. Effects of prenatal malnutrition and postnatal nutritional rehabilitation on CA3 hippocampal pyramidal cells in rats of four ages. Brain Res. 1994;662(1–2):117–26.
  • Luebke J, St John J, Galler JR. Prenatal protein malnutrition results in increased frequency of miniature inhibitory synaptic currents in rat CA1 pyramidal cells. Synapse. 2000;37(1):23–31.
  • Lister JP, Blatt GJ, DeBassio WA, Kemper TL, Tonkiss J, Galler JR, Rosene DL. Effect of prenatal protein malnutrition on numbers of neurons in the principal cell layers of the adult rat hippocampal formation. Hippocampus. 2005;15(3):393–403.
  • Díaz-Cintra S, González-Maciel A, Morales MA, Aguilar A, Cintra L, Prado-Alcalá RA. Protein malnutrition differentially alters the number of glutamic acid decarboxylase-67 interneurons in dentate gyrus and CA1-3 subfields of the dorsal hippocampus. Exp Neurol. 2007;208(1):47–53.
  • Lister JP, Blatt GJ, Kemper TL, Tonkiss J, DeBassio WA, Galler JR, Rosene DL. Prenatal protein malnutrition alters the proportion but not numbers of parvalbumin-immunoreactive interneurons in the hippocampus of the adult Sprague-Dawley rat. Nutr Neurosci. 2011;14(4):165–78.
  • Lister JP, Tonkiss J, Blatt GJ, Kemper TL, DeBassio WA, Galler JR, Rosene DL. Asymmetry of neuron numbers in the hippocampal formation of prenatally malnourished and normally nourished rats: a stereological investigation. Hippocampus. 2006;16(11):946–58.
  • Tonkiss J, Foster GA, Galler JR. Prenatal protein malnutrition and hippocampal function: partial reinforcement extinction effect. Behav Brain Res. 1991;27:809–13.
  • Rosene DL, Roy NJ, Davis BJ. A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. J Histochem Cytochem. 1986;34(10):1301–15.
  • Rosene DL, Lister JP, Schwagerl AL, Tonkiss J, McCormick CM, Galler JR. Prenatal protein malnutrition in rats alters the c-Fos response of neurons in the anterior cingulate and medial prefrontal region to behavioral stress. Nutr Neurosci. 2004;7(5–6):281–9.
  • Haug FM. Sulphide silver pattern and cytoarchitectonics of parahippocampal areas in the rat. Special reference to the subdivision of area entorhinalis (area 28) and its demarcation from the pyriform cortex. Adv Anat Embryol Cell Biol. 1976;52(4):3–73.
  • Mulders WH, West MJ, Slomianka L. Neuron numbers in the presubiculum, parasubiculum, and entorhinal area of the rat. J Comp Neurol. 1997;385(1):83–94.
  • Witter MP, Wouterlood FG, Naber PA, Van Haeften T. Anatomical organization of the parahippocampal-hippocampal network. Ann N Y Acad Sci. 2000;911(1):1–24.
  • van Groen T, Wyss JM. The postsubicular cortex in the rat: characterization of the fourth region of the subicular cortex and its connections. Brain Res. 1990;529(1–2):165–77.
  • Ding S-L. Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent. J Comp Neurol. 2013;521(18):4145–62.
  • West MJ, Slomianka L, Gundersen HJ. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec. 1991;231(4):482–97.
  • Gundersen HJ, Jensen EB. The efficiency of systematic sampling in stereology and its prediction. J Microsc. 1987;147(Pt 3):229–63.
  • Gundersen HJG, Jensen EBV, Kieu K, Nielsen J. The efficiency of systematic sampling in stereology - reconsidered. J Microsc. 1999;193(3):199–211.
  • Cruz-Rizzolo RJ, Limieri LL, de Paiva IR, Ribeiro JOB, Pimenta TF, Pinato L, et al. Protein malnutrition during gestation and early life decreases neuronal size in the medial prefrontal cortex of post-pubertal rats. IBRO Rep. 2017;3:65–71.
  • Owen AM, Roberts AC, Polkey CE, Sahakian BJ, Robbins TW. Extra-dimensional versus intra-dimensional set shifting performance following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia. 1991;29(10):993–1006.
  • Tomita H, Ohbayashi M, Nakahara K, Hasegawa I, Miyashita Y. Top-down signal from prefrontal cortex in executive control of memory retrieval. Nature. 1999;401(6754):699–703.
  • Baldauf D, Desimone R. Neural mechanisms of object-based attention. Science. 2014;344(6182):424–7.
  • Chudasama Y, Passetti F, Rhodes SEV, Lopian D, Desai A, Robbins TW. 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. 2003;146(1–2):105–19.
  • Cenquizca LA, Swanson LW. Analysis of direct hippocampal cortical field CA1 axonal projections to diencephalon in the rat. J Comp Neurol. 2006;497(1):101–14.
  • Kerr KM, Agster KL, Furtak SC, Burwell RD. Functional neuroanatomy of the parahippocampal region: the lateral and medial entorhinal areas. Hippocampus. 2007;17(9):697–708.
  • Chudasama Y, Doobay VM, Liu Y. Hippocampal-prefrontal cortical circuit mediates inhibitory response control in the rat. J Neurosci. 2012;32(32):10915–24.
  • Floyd NS, Price JL, Ferry AT, Keay KA, Bandler R. Orbitomedial prefrontal cortical projections to hypothalamus in the rat. J Comp Neurol. 2001;432(3):307–28.
  • Herman JP, Ostrander MM, Mueller NK, Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry. 2005;29(8):1201–13.
  • Newman LA, Baraiolo J, Mokler DJ, Rabinowitz AG, Galler JR, McGaughy JA. Prenatal protein malnutrition produces resistance to distraction similar to noradrenergic deafferentation of the prelimbic cortex in a sustained attention task. Front Neurosci. 2019;13:123. doi:10.3389/fnins.2019.00123.
  • Xiang L, Harel A, Gao H, Pickering AE, Sara SJ, Wiener SI. Behavioral correlates of activity of optogenetically identified locus coeruleus noradrenergic neurons in rats performing T-maze tasks. Sci Rep. 2019;9(1):1361.
  • Mokler DJ, Torres OI, Galler JR, Morgane PJ. Stress-induced changes in extracellular dopamine and serotonin in the medial prefrontal cortex and dorsal hippocampus of prenatally malnourished rats. Brain Res. 2007;1148:226–33.
  • Tolman EC. Cognitive maps in rats and men. Psychol Rev. 1948;55(4):189–208.
  • O’Keefe J, Nadal L. The hippocampus as a cognitive. Map: Oxford University; 1978.
  • McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser M-B. Path integration and the neural basis of the “cognitive map”. Nat Rev Neurosci. 2006;7(8):663–78.
  • Hafting T, Fyhn M, Molden S, Moser M-B, Moser EI. Microstructure of a spatial map in the entorhinal cortex. Nature. 2005;436(7052):801–6.
  • Taube JS. The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci. 2007;30:181–207.
  • Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser M-B. Grid cells in pre- and parasubiculum. Nat Neurosci. 2010;13(8):987–94.
  • Tonkiss J, Shultz P, Galler JR. An analysis of spatial navigation in prenatally protein malnourished rats. Physiol Behav. 1994;55(2):217–24.
  • Tonkiss J, Shultz PL, Shumsky JS, Galler JR. Development of spatial navigation following prenatal cocaine and malnutrition in rats: lack of additive effects. Neurotoxicol Teratol. 1997;19(5):363–72.
  • Tonkiss J, Shultz PL, Bonnie KE, Hudson JL, Duran P, Galler JR. Spatial learning deficits induced by muscimol and CL218,872: lack of effect of prenatal malnutrition. Nutr Neurosci. 2003;6(6):379–87.
  • Shumsky JS, Shultz PL, Galler JR, Tonkiss J. Differential effects of prenatal protein malnutrition and prenatal cocaine on radial arm maze performance in adult male rats. Nutr Neurosci. 1999;2(2):113–22.
  • Nagahara AH, Otto T, Gallagher M. Entorhinal-perirhinal lesions impair performance of rats on two versions of place learning in the Morris water maze. Behav Neurosci. 1995;109(1):3–9.
  • Steffenach H-A, Witter M, Moser M-B, Moser EI. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron. 2005;45(2):301–13.
  • Suh J, Rivest AJ, Nakashiba T, Tominaga T, Tonegawa S. Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science. 2011;334(6061):1415–20.
  • Pastalkova E, Itskov V, Amarasingham A, Buzsáki G. Internally generated cell assembly sequences in the rat hippocampus. Science. 2008;321(5894):1322–7.
  • MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H. Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron. 2011;71(4):737–49.
  • Rueckemann JW, Sosa M, Giocomo LM, Buffalo EA. The grid code for ordered experience. Nat Rev Neurosci. 2021;22(10):637–49.
  • Kraus BJ, Robinson 2nd RJ, White JA, Eichenbaum H, Hasselmo ME. Hippocampal “time cells”: time versus path integration. Neuron. 2013;78(6):1090–101.
  • Kraus BJ, Brandon MP, Robinson 2nd RJ, Connerney MA, Hasselmo ME, Eichenbaum H. During running in place, grid cells integrate elapsed time and distance run. Neuron. 2015;88(3):578–89.
  • Rueckemann JW, Buffalo EA. Spatial responses, immediate experience, and memory in the monkey hippocampus. Curr Opin Behav Sci. 2017;17:155–60.
  • Bronzino JD, Austin-LaFrance RJ, Morgane PJ. Effects of prenatal protein malnutrition on perforant path kindling in the rat. Brain Res. 1990;515(1–2):45–50.
  • Bronzino JD, Austin-LaFrance RJ, Morgane PJ, Galler JR. Effects of prenatal protein malnutrition on kindling-induced alterations in dentate granule cell excitability. II. Paired-pulse measures. Exp Neurol. 1991c;112(2):216–23.
  • Bronzino Joseph D, Austin-LaFrance RJ, Morgane PJ, Galler JR. Effects of prenatal protein malnutrition on kindling-induced alterations in dentate granule cell excitability. Exp Neurol. 1991a;112(2):216–23. doi:10.1016/0014-4886(91)90072-k.
  • Bronzino JD, Austin-LaFrance RJ, Morgane PJ, Galler JR. Effects of prenatal protein malnutrition on kindling-induced alterations in dentate granule cell excitability. I. Synaptic transmission measures. Exp Neurol. 1991b;112(2):206–15.
  • Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL. Alzheimer’s disease: cell-specific pathology isolates the hippocampal formation. Science. 1984;225(4667):1168–70.
  • Arnold SE, Hyman BT, Flory J, Damasio AR, Van Hoesen GW. The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer’s disease. Cereb Cortex. 1991;1(1):103–16.
  • Braak H, Braak E. Entorhinal-hippocampal interaction in mnestic disorders. Hippocampus. 1993;3(S1):239–46.
  • Gomez-Isla T, West HL, Rebeck GW, Harr SD, Growdon JH, Locascio JJ, et al. Clinical and pathological correlates of apolipoprotein E epsilon 4 in Alzheimer’s disease. Ann Neurol. 1996;39(1):62–70.
  • Kordower JH, Chu Y, Stebbins GT, DeKosky ST, Cochran EJ, Bennett D, Mufson EJ. Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment. Ann Neurol. 2001;49(2):202–13.
  • Du F, Whetsell Jr WO, Abou-Khalil B, Blumenkopf B, Lothman EW, Schwarcz R. Preferential neuronal loss in layer III of the entorhinal cortex in patients with temporal lobe epilepsy. Epilepsy Res. 1993;16(3):223–33.
  • Du F, Eid T, Lothman EW, Köhler C, Schwarcz R. Preferential neuronal loss in layer III of the medial entorhinal cortex in rat models of temporal lobe epilepsy. J Neurosci. 1995;15(10):6301–13.
  • Slomianka L. Neurons of origin of zinc-containing pathways and the distribution of zinc-containing boutons in the hippocampal region of the rat. Neuroscience. 1992;48(2):325–52.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.