Skip to main content

Advertisement

Log in

Spatial reversal learning is impaired by age in pet dogs

  • Published:
AGE Aims and scope Submit manuscript

Abstract

Aged dogs spontaneously develop progressive decline in both cognitive and behavioral function, in addition to neuropathological changes, that collectively parallel several aspects of human aging and Alzheimer’s disease progression and likely contribute to the development of canine cognitive dysfunction syndrome. In the current study, ethologically relevant spatial learning, retention, and reversal learning tasks were conducted, with the goal of expanding canine neuropsychological testing to pet dogs. Initially, dogs (N = 44, aged 7.8 ± 2.8 years, mean ± SD) had to learn which of two alternative routes successfully led out of a T-maze. Two weeks later, long-term memory retention was assessed, immediately followed by a reversal learning task in which the previously correct route out of the maze was reversed compared with the initial learning and memory retention tasks. No effects of age were evident on the learning or retention tasks. However, older (≥8 years) dogs were significantly impaired on the reversal learning task compared with younger ones (<8 years). Moreover, trial response latency was significantly increased in aged dogs across both the initial and reversal learning tasks but not on the retention task, which suggests that processing speed was impaired by increasing age during the acquisition of novel spatial information but not during performance of previously learned responses. Overall, the current study provides a framework for assessing cognitive function in pet dogs, which should improve understanding of the effects of aging on cognition in the dog population.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

AD:

Alzheimer’s disease

Aβ:

β-amyloid

References

  • Adams B, Chan A, Callahan H, Milgram NW (2000) The canine as a model of human cognitive aging: recent developments. Prog Neuropsychopharmacol Biol Psychiatry 24:675–692

    Article  PubMed  CAS  Google Scholar 

  • Araujo JA, Studzinski CM, Milgram NW (2005) Further evidence for the cholinergic hypothesis of aging and dementia from the canine model of aging. Prog Neuropsychopharmacol Biol Psychiatry 29:411–422. doi:10.1016/j.pnpbp.2004.12.008

    Article  PubMed  CAS  Google Scholar 

  • Ashton RL, De Lillo C (2011) Association, inhibition, and object permanence in dogs' (Canis familiaris) spatial search. J Comp Psychol 125:194–206. doi:10.1037/a0022584

    Article  PubMed  Google Scholar 

  • Begega A, Cienfuegos S, Rubio S, Santin JL, Miranda R, Arias JL (2001) Effects of ageing on allocentric and egocentric spatial strategies in the Wistar rat. Behav Processes 53:75–85. doi:10.1016/s0376-6357(00)00150-9

    Article  PubMed  Google Scholar 

  • Borras D, Ferrer I, Pumarola M (1999) Age-related changes in the brain of the dog. Vet Pathol 36:202–211. doi:10.1354/vp.36-3-202

    Article  PubMed  CAS  Google Scholar 

  • Braak H, Braak E (1991) Neuropathological staging of alzheimer-related changes. Acta Neuropathol (Berl) 82:239–259

    Article  CAS  Google Scholar 

  • Carrillo-Mora P, Giordano M, Santamaria A (2009) Spatial memory: theoretical basis and comparative review on experimental methods in rodents. Behav Brain Res 203:151–164. doi:10.1016/j.bbr.2009.05.022

    Article  Google Scholar 

  • Christie LA, Studzinski CM, Araujo JA, Leung CSK, Ikeda-Douglas CJ, Head E, Cotman CW, Milgram NW (2005) A comparison of egocentric and allocentric age-dependent spatial learning in the beagle dog. Prog Neuropsychopharmacol Biol Psychiatry 29:361–369. doi:10.1016/j/pnpbp.2004.12.002

    Article  PubMed  Google Scholar 

  • Cotman CW, Head E (2008) The canine (dog) model of human aging and disease: dietary, environmental and immunotherapy approaches. J Alzheimer Dis 15:685–707

    CAS  Google Scholar 

  • Cushman LA, Stein K, Duffy CJ (2008) Detecting navigational deficits in cognitive aging and Alzheimer disease using virtual reality. Neurology 71:888–895. doi:10.1212/01.wnl.0000326262.67613.fe

    Article  PubMed  Google Scholar 

  • Fiset S (2007) Landmark-based search memory in the domestic dog (Canis familiaris). J Comp Psychol 121:345–353. doi:10.1037/0735-7036.121.4.345

    Article  PubMed  Google Scholar 

  • Fiset S, Beaulieu C, Landry F (2003) Duration of dogs' (Canis familiaris) working memory in search for disappearing objects. Anim Cogn 6:1–10. doi:10.1007/S10071-002-0157-4

    PubMed  Google Scholar 

  • Gallagher M, Pelleymounter MA (1988) An age-related spatial-learning deficit—choline uptake distinguishes impaired and unimpaired rats. Neurobiol Aging 9:363–369. doi:10.1016/s0197-4580(88)80082-4

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Soriano J, Garcia PM, Contreras-Rodriguez J, Martinez-Sainz P, Rodriguez-Veiga E (2001) Age-related changes in the ventricular system of the dog brain. Anat Anz 183:283–291. doi:10.1016/s0940-9602(01)80236-3

    Article  CAS  Google Scholar 

  • Head E, Callahan H, Muggenburg BA, Cotman CW, Milgram NW (1998) Visual-discrimination learning ability and beta-amyloid accumulation in the dog. Neurobiol Aging 19:415–425

    Article  PubMed  CAS  Google Scholar 

  • Head E, McCleary R, Hahn FF, Milgram NW, Cotman CW (2000) Region-specific age at onset of beta-amyloid in dogs. Neurobiol Aging 21:89–96

    Article  PubMed  CAS  Google Scholar 

  • Head E, Liu J, Hagen TM, Muggenburg BA, Milgram NW, Ames BN, Cotman CW (2002) Oxidative damage increases with age in a canine model of human brain aging. J Neurochem 82:375–381

    Article  PubMed  CAS  Google Scholar 

  • Herndon JG, Moss MB, Rosene DL, Killiany RJ (1997) Patterns of cognitive decline in aged rhesus monkeys. Behav Brain Res 87:25–34. doi:10.1016/s0166-4328(96)02256-5

    Article  PubMed  CAS  Google Scholar 

  • Hort J, Laczo J, Vyhnalek M, Bojar M, Bures J, Vlcek K (2007) Spatial navigation deficit in amnestic mild cognitive impairment. Proc Natl Acad Sci U S A 104:4042–4047. doi:10.1073/pnas.0611314104

    Article  PubMed  CAS  Google Scholar 

  • Iachini I, Iavarone A, Senese VP, Ruotolo F, Ruggiero G (2009) Visuospatial memory in healthy elderly, AD and MCI: a review. Curr Aging Sci 2:43–59

    PubMed  Google Scholar 

  • Ingram DK (1988) Complex maze-learning in rodents as a model of age-related memory impairment. Neurobiol Aging 9:475–485. doi:10.1016/s0197-4580(88)80101-5

    Article  PubMed  CAS  Google Scholar 

  • Klein DA, Steinberg M, Galik E, Steele C, Sheppard JM, Warren A, Rosenblatt A, Lyketsos CG (1999) Wandering behaviour in community-residing persons with dementia. Int J Geriatr Psychiatry 14:272–279. doi:10.1002/(sici)1099-1166(199904)14:4<272::aid-gps896>3.0.co;2-P

    Article  PubMed  CAS  Google Scholar 

  • Lai ZC, Moss MB, Killiany RJ, Rosene DL, Herndon JG (1995) Executive system dysfunction in the aged monkey—spatial and object reversal-learning. Neurobiol Aging 16:947–954. doi:10.1016/0197-4580(95)02014-4

    Article  PubMed  CAS  Google Scholar 

  • Landsberg G (2005) Therapeutic agents for the treatment of cognitive dysfunction syndrome in senior dogs. Prog Neuropsychopharmacol Biol Psychiatry 29:471–479. doi:10.1016/j.pnpbp.2004.12.012

    Article  PubMed  CAS  Google Scholar 

  • Landsberg GM, Nichol J, Araujo JA (2012) Cognitive dysfunction syndrome: a disease of canine and feline brain ageing. Vet Clin N Am Sm Anim Pract 42:749–768. doi: 10.1016/j.cvsm.2012.04.003

  • Lukoyanov NV, Andrade JP, Madeira MD, Paula-Barbosa MM (1999) Effects of age and sex on the water maze performance and hippocampal cholinergic fibers in rats. Neurosci Lett 269:141–144. doi:10.1016/s0304-3940(99)00442-5

    Article  PubMed  CAS  Google Scholar 

  • McLay RN, Freeman SM, Harlan RE, Kastin AJ, Zadina JE (1999) Tests used to assess the cognitive abilities of aged rats: their relation to each other and to hippocampal morphology and neurotrophin expression. Gerontology 45:143–155. doi:10.1159/000022077

    Article  PubMed  CAS  Google Scholar 

  • Miklosi A (2009) Dog behaviour, evolution and cognition. Oxford University Press, New York, pp 137–150

    Google Scholar 

  • Milgram NW, Head E, Weiner E, Thomas E (1994) Cognitive functions and aging in the dog—acquisition of nonspatial visual tasks. Behav Neurosci 108:57–68

    Article  PubMed  CAS  Google Scholar 

  • Milgram NW, Head E, Muggenburg B, Holowachuk D, Murphey H, Estrada J, Ikeda-Douglas CJ, Zicker SC, Cotman CW (2002a) Landmark discrimination learning in the dog: effects of age, an antioxidant fortified food, and cognitive strategy. Neurosci Biobehav Rev 26:679–695

    Article  PubMed  Google Scholar 

  • Milgram NW, Zicker SC, Head E, Muggenburg BA, Murphey H, Ikeda-Douglas CJ, Cotman CW (2002b) Dietary enrichment counteracts age-associated cognitive dysfunction in canines. Neurobiol Aging 23:737–745

    Article  PubMed  CAS  Google Scholar 

  • Moffat SD (2009) Aging and spatial navigation: what do we know and where do we go. Neuropsychol Rev 19:478–489. doi:10.1007/s11065-009-9120-3

    Article  PubMed  Google Scholar 

  • Morys J, Narkiewicz O, Maciejewska B, Wegiel J, Wisniewski HM (1994) Amyloid deposits and loss of neurons in the claustrum of the aged dog. Neuroreport 5:1825–1828. doi:10.1097/00001756-199409080-00035

    Article  PubMed  CAS  Google Scholar 

  • Newman MC, Kaszniak AW (2000) Spatial memory and aging: performance on a human analog of the Morris water maze. Aging Neuropsychol Cogn 7:86–93. doi:10.1076/1382-5585(200006)7:2;1-u;ft086

    Article  Google Scholar 

  • Osella MC, Re G, Odore R, Girardi C, Badino P, Barbero R, Bergamasco L (2007) Canine cognitive dysfunction syndrome: prevalence, clinical signs and treatment with a neuroprotective nutraceutical. Appl Anim Behav Sci 105:297–310. doi:10.1016/j.applanim.2006.11.007

    Article  Google Scholar 

  • Papaioannou N, Tooten PCJ, van Ederen AM, Bohl JRE, Rofina J, Tsangaris T, Gruys E (2001) Immunohistochemical investigation of the brain of aged dogs. I. Detection of neurofibrillary tangles and of 4-hydroxynonenal protein, an oxidative damage product, in senile plaques. Amyloid 8:11–21. doi:10.3109/13506120108993810

    Article  PubMed  CAS  Google Scholar 

  • Pongracz P, Miklosi A, Kubinyi E, Gurobi K, Topal J, Csanyi V (2001) Social learning in dogs: the effect of a human demonstrator on the performance of dogs in a detour task. Anim Behav 62:1109–1117. doi:10.1006/anbe.2001.1866

    Article  Google Scholar 

  • Rahner-Welsch S, Frolich L, Stoll S, Hoyer S (1995) Decline and preservation of reversal-learning abilities and acquisition in the course of senescence. Neurosci Lett 194:121–123. doi:10.1016/0304-3940(95)11712-6

    Article  PubMed  CAS  Google Scholar 

  • Regolin L, Rose SPR (1999) Long-term memory for a spatial task in young chicks. Anim Behav 57:1185–1191

    Article  PubMed  Google Scholar 

  • Regolin L, Vallortigara G, Zanforlin M (1995) Object and spatial representations in detour problems by chicks. Anim Behav 49:195–199

    Article  Google Scholar 

  • Rofina JE, Singh K, Skoumalova-Vesela A, van Ederen AM, van Asten A, Wilhelm J, Gruys E (2004) Histochemical accumulation of oxidative damage products is associated with Alzheimer-like pathology in the canine. Amyloid 11:90–100. doi:10.1080/13506120412331285779

    Article  PubMed  CAS  Google Scholar 

  • Ruehl WW, Bruyette DS, DePaoli A, Cotman CW, Head E, Milgram NW, Cummings BJ (1995) Canine cognitive dysfunction as a model for human age-related cognitive decline, dementia and Alzheimer's disease: clinical presentation, cognitive testing, pathology and response to 1-deprenyl therapy. Prog Brain Res 106:217–225

    Article  PubMed  CAS  Google Scholar 

  • Salvin HE, McGreevy PD, Sachdev PS, Valenzuela MJ (2011) The canine sand maze: an appetitive spatial memory paradigm sensitive to age-related change in dogs. J Exp Anal Behav 95:109–118. doi:10.1901/jeab.2011.95-109

    Article  PubMed  Google Scholar 

  • Sharma S, Rakoczy S, Brown-Borg H (2010) Assessment of spatial memory in mice. Life Sci 87:521–536. doi:10.1016/j.lfs.2010.09.004

    Article  PubMed  CAS  Google Scholar 

  • Siwak CT, Tapp PD, Milgram NW (2001) Effect of age and level of cognitive function on spontaneous and exploratory Behaviors in the beagle dog. Learn Mem 8:317–325. doi:10.1101/lm.41701

    Article  PubMed  CAS  Google Scholar 

  • Siwak-Tapp CT, Head E, Muggenburg BA, Milgram NW, Cotman CW (2008) Region specific neuron loss in the aged canine hippocampus is reduced by enrichment. Neurobiol Aging 29:39–50. doi:10.1016/j.neurobiolaging.2006.09.018

    Article  PubMed  Google Scholar 

  • Stephens DN, Weidmann R, Quartermain D, Sarter M (1985) Reversal-learning in senescent rats. Behav Brain Res 17:193–202. doi:10.1016/0166-4328(85)90043-9

    Article  PubMed  CAS  Google Scholar 

  • Studzinski CM, Araujo JA, Milgram NW (2005) The canine model of human cognitive aging and dementia: pharmacological validity of the model for assessment of human cognitive-enhancing drugs. Prog Neuropsychopharmacol Biol Psychiatry 29:489–498. doi:10.1016/j.pnpbp.2004.12.014

    Article  PubMed  CAS  Google Scholar 

  • Studzinski CM, Christie LA, Araujo JA, Burnham WM, Head E, Cotman CW, Milgram NW (2006) Visuospatial function in the beagle dog: an early marker of cognitive decline in a model of human aging and dementia. Neurobiol Learn Mem 86:197–204. doi:10.1016/j.nlm.2006.02.005

    Article  PubMed  Google Scholar 

  • Su MY, Tapp PD, Vu L, Chen YF, Chu Y, Muggenburg B, Chiou JY, Chen CQ, Wang J, Bracco C, Head E (2005) A longitudinal study of brain morphometrics using serial magnetic resonance imaging analysis in a canine model of aging. Prog Neuropsychopharmacol Biol Psychiatry 29:389–397. doi:10.1016/j.pnpbp.2004.12.005

    Article  PubMed  Google Scholar 

  • Tapp PD, Siwak CT, Estrada J, Head E, Muggenburg BA, Cotman CW, Milgram NW (2003a) Size and reversal learning in the beagle dog as a measure of executive function and inhibitory control in aging. Learn Memory 10:64–73. doi:10.1101/lm.54403

    Article  Google Scholar 

  • Tapp PD, Siwak CT, Estrada J, Holowachuk D, Milgram NW (2003b) Effects of age on measures of complex working memory span in the beagle dog (Canis familiaris) using two versions of a spatial list learning paradigm. Learn Memory 10:148–160. doi:10.1101/lm.56503

    Article  Google Scholar 

  • Tapp D, Chu Y, Vu L, Chiou JY, Milgram NW, Nalcioglu O, Su MY (2004) Age-dependent changes in regional brain volume and cerebral blood volume in white matter of the canine brain measured using dynamic susceptibility contrast MRI. Neurobiol Aging 25:S380–S381

    Article  Google Scholar 

  • Tapp PD, Chu Y, Araujo JA, Chiou JY, Head E, Milgram NW, Su MY (2005) Effects of scopolamine challenge on regional cerebral blood volume. A pharmacological model to validate the use of contrast enhanced magnetic resonance imaging to assess cerebral blood volume in a canine model of aging. Prog Neuropsychopharmacol Biol Psychiatry 29:399–406. doi:10.1016/j.pnpbp.2004.12.006

    Article  PubMed  CAS  Google Scholar 

  • Tolman EC, Honzik CH (1930) Introduction and removal of reward, and maze performance in rats. Univ Calif Pub Psychol 4:257–275

    Google Scholar 

  • Tsuchida J, Kubo N, Kojima S (2002) Position reversal learning in aged Japanese macaques. Behav Brain Res 129:107–112. doi:10.1016/s0166-4328(01)00336-9

    Article  PubMed  Google Scholar 

  • Uchida K, Nakayama H, Tateyama S, Goto N (1992) Immunohistochemical analysis of constituents of senile plaques and cerebrovascular amyloid in aged dogs. J Vet Med Sci 54:1023–1029

    Article  PubMed  CAS  Google Scholar 

  • Voytko ML (1999) Impairments in acquisition and reversals of two-choice discriminations by aged rhesus monkeys. Neurobiol Aging 20:617–627. doi:10.1016/s0197-4580(99)00097-4

    Article  PubMed  CAS  Google Scholar 

  • Waters D (2011) Aging research 2011: exploring the pet dog paradigm. ILAR J 52:97–105

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paolo Mongillo.

About this article

Cite this article

Mongillo, P., Araujo, J.A., Pitteri, E. et al. Spatial reversal learning is impaired by age in pet dogs. AGE 35, 2273–2282 (2013). https://doi.org/10.1007/s11357-013-9524-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11357-013-9524-0

Keywords

Navigation