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Experiments with insects and crabs have demonstrated their remarkable capacity to learn and memorize complex visual features (Giurfa et al., 2001; Pedreira and Maldonado, 2003; Chittka and Niven, 2009). Such abilities are thought to require modular brain processing similar to that occurring in vertebrates (Menzel and Giurfa, 2001). Yet, physiological evidence for this type of functioning in the small brains of arthropods is still scarce (Liu et al., 1999, 2006; Menzel and Giurfa, 2001). In the crab Chasmagnathus granulatus, the learning rate as well as the long-term memory of a visual stimulus has been found to be reflected in the performance of identified lobula giant neurons (LGs) (Tomsic et al., 2003). The memory can only be evoked in the training context, indicating that animals store two components of the learned experience, one related to the visual stimulus and one related to the visual context (Tomsic et al., 1998; Hermitte et al., 1999). By performing intracellular recordings in the intact animal, we show that the ability of crabs to generalize the learned stimulus into new space positions and to distinguish it from a similar but unlearned stimulus, two of the main attributes of stimulus memory, is reflected by the performance of the LGs. Conversely, we found that LGs do not support the visual context memory component. Our results provide physiological evidence that the memory traces regarding "what" and "where" are stored separately in the arthropod brain. © 2011 the authors.


Documento: Artículo
Título:Brain modularity in arthropods: Individual neurons that support "what" but not "where" memories
Autor:Sztarker, J.; Tomsic, D.
Filiación:Laboratorio de Neurobiología de la Memoria, Departamento Fisiología, Biología, Universidad de Buenos Aires, Instituto de Fisiologia, Biologia Molecular y Neurociencias, Consejo, Pabellón 2 Ciudad Universitaria, Intendente Güiraldes 2160, Buenos Aires 1428, Argentina
Departamento Biodiversidad y Biología Evolutiva, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellon 2 Ciudad Universitaria, Ing. Guiraldes 2160, Buenos Aires 1428, Argentina
Palabras clave:animal behavior; animal experiment; article; brain function; controlled study; crab; learning; long term memory; male; memory consolidation; nerve cell network; neuromodulation; neurotransmission; nonhuman; priority journal; stimulus response; task performance; visual stimulation; Action Potentials; Animals; Brachyura; Generalization, Stimulus; Learning; Male; Memory; Neurons; Photic Stimulation
Página de inicio:8175
Página de fin:8180
Título revista:Journal of Neuroscience
Título revista abreviado:J. Neurosci.


  • Benard, J., Stach, S., Giurfa, M., Categorization of visual stimuli in the honeybee Apis mellifera (2006) Anim Cogn, 9, pp. 257-270
  • Chittka, L., Niven, J., Are bigger brains better? (2009) Curr Biol, 19, pp. R995-R1008
  • Frenkel, L., Freudenthal, R., Romano, A., Nahmod, V.E., Maldonado, H., Delorenzi, A., Angiotensin II and the transcription factor Rel/NF-kappaB link environmental water shortage with memory improvement (2002) Neuroscience, 115, pp. 1079-1087
  • Giurfa, M., Eichmann, B., Menzel, R., Symmetry perception in an insect (1996) Nature, 382, pp. 458-461
  • Giurfa, M., Zhang, S., Jenett, A., Menzel, R., Srinivasan, M.V., The concepts of "sameness" and "difference" in an insect (2001) Nature, 410, pp. 930-933
  • Hemmi, J.M., Merkle, T., High stimulus specificity characterizes anti-predator habituation under natural conditions (2009) Proc Biol Sci, 276, pp. 4381-4388
  • Hermitte, G., Pedreira, M.E., Tomsic, D., Maldonado, H., Context shift and protein synthesis inhibition disrupt long-term habituation after spaced, but not massed training in the crab Chasmagnathus (1999) Neurobiol Learn Mem, 71, pp. 34-49
  • Kelly, D.D., Stress-induced analgesia (1986) Annals of the New York Academy of Science, 467. , New York: New York Academy of Science
  • Li, N., Cox, D.D., Zoccolan, D., Dicarlo, J.J., What response properties do individual neurons need to underlie position and clutter "invariant" object recognition? (2009) J Neurophysiol, 102, pp. 360-376
  • Liu, G., Seiler, H., Wen, A., Zars, T., Ito, K., Wolf, R., Heisenberg, M., Liu, L., Distinct memory traces for two visual features in the Drosophila brain (2006) Nature, 439, pp. 551-556
  • Liu, L., Wolf, R., Ernst, R., Heisenberg, M., Context generalization in Drosophila visual learning requires the mushroom bodies (1999) Nature, 400, pp. 753-756
  • Lozada, M., Romano, A., Maldonado, H., Long term habituation to a danger stimulus in the crab Chasmagnathus granulatus (1990) Physiol Behav, 47, pp. 35-41
  • McKinzie, M.E., Benton, J.L., Beltz, B.S., Mellon, D., Parasol cells of the hemiellipsoid body in the crayfish Procambarus clarkii: Dendritic branching patterns and functional implications (2003) J Comp Neurol, 462, pp. 168-179
  • McLaughlin, J.P., Marton-Popovici, M., Chavkin, C., Kappa opioid receptor antagonism and prodynorphin gene disruption block stressinduced behavioral responses (2003) J Neurosci, 23, pp. 5674-5683
  • Medan, V., Oliva, D., Tomsic, D., Characterization of interneurons responsive to visual stimuli that elicit escape behaviors in the crab Chasmagnathus (2007) J Neurophysiol, 98, pp. 2414-2428
  • Menzel, R., Searching for the memory trace in a mini-brain, the honeybee (2001) Learn Mem, 8, pp. 53-62
  • Menzel, R., Giurfa, M., Cognitive architecture of a mini-brain: The honeybee (2001) Trends Cogn Sci, 5, pp. 62-71
  • Mizunami, M., Weibrecht, J.M., Strausfeld, N.J., Mushroom bodies of the cockroach: Their participation in place memory (1998) J Comp Neurol, 402, pp. 520-537
  • Oliva, D., Medan, V., Tomsic, D., Escape behavior and neuronal responses to looming stimuli in the crab Chasmagnathus granulatus (Decapoda: Grapsidae) (2007) J Exp Biol, 210, pp. 865-880
  • Pedreira, M.E., Maldonado, H., Protein synthesis subserves reconsolidation or extintion depending on reminder duration (2003) Neuron, 38, pp. 863-869
  • Pedreira, M.E., Pérez-Cuesta, L.M., Maldonado, H., Reactivation and reconsolidation of long-term memory in the crab Chasmagnathus: Protein synthesis requirement and mediation by NMDA-type glutamatergic receptors (2002) J Neurosci, 22, pp. 8305-8311
  • Romano, A., Lozada, M., Maldonado, H., Nonhabituation processes affect stimulus specificity of response habituation in the crab Chasmagnathus granulatus (1991) Behav Neurosci, 105, pp. 542-552
  • Sztarker, J., Tomsic, D., Binocular visual integration in the crustacean nervous system (2004) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 190, pp. 951-962
  • Sztarker, J., Tomsic, D., Neuronal correlates of the visually elicited escape response of the crab Chasmagnathus upon seasonal variations, stimuli changes and perceptual alterations (2008) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 194, pp. 587-596
  • Sztarker, J., Strausfeld, N.J., Tomsic, D., Organization of the optic lobes that support motion detection in a semiterrestrial crab (2005) J Comp Neurol, 493, pp. 396-411
  • Tang, S., Wolf, R., Xu, S., Heisenberg, M., Visual pattern recognition in Drosophila is invariant for retinal position (2004) Science, 305, pp. 1020-1022
  • Tibbetts, E.A., Dale, J., A socially enforced signal of quality in a paper wasp (2004) Nature, 432, pp. 218-222
  • Tomsic, D., Massoni, V., Maldonado, H., Habituation to a danger stimulus in two semiterrestrial crabs. Ontogenic, ecological and opioid system correlates (1993) J Comp Physiol a Neuroethol Sens Neural Behav Physiol, 173, pp. 621-633
  • Tomsic, D., Pedreira, M.E., Romano, A., Hermitte, G., Maldonado, H., Context-US association as a determinant of long-term habituation in the crab Chasmagnathus (1998) Anim Learn Behav, 26, pp. 196-209
  • Tomsic, D., de Astrada, B.M., Sztarker, J., Identification of individual neurons reflecting short- and long-term visual memory in an arthropod (2003) J Neurosci, 23, pp. 8539-8546
  • Valeggia, C., Fernandez-Duque, E., Maldonado, H., Danger stimulusinduced analgesia in the crab Chasmagnathus granulatus (1989) Brain Res, 481, pp. 304-308
  • Wehner, R., Pattern recognition (1974) The Compound Eye and Vision of Insects, pp. 75-113. , Horridge GA, Oxford: Clarendon
  • Weinberger, N.M., Miasnikov, A.A., Chen, J.C., Sensory memory consolidation observed: Increased specificity of detail over days (2009) Neurobiol Learn Mem, 91, pp. 273-286


---------- APA ----------
Sztarker, J. & Tomsic, D. (2011) . Brain modularity in arthropods: Individual neurons that support "what" but not "where" memories. Journal of Neuroscience, 31(22), 8175-8180.
---------- CHICAGO ----------
Sztarker, J., Tomsic, D. "Brain modularity in arthropods: Individual neurons that support "what" but not "where" memories" . Journal of Neuroscience 31, no. 22 (2011) : 8175-8180.
---------- MLA ----------
Sztarker, J., Tomsic, D. "Brain modularity in arthropods: Individual neurons that support "what" but not "where" memories" . Journal of Neuroscience, vol. 31, no. 22, 2011, pp. 8175-8180.
---------- VANCOUVER ----------
Sztarker, J., Tomsic, D. Brain modularity in arthropods: Individual neurons that support "what" but not "where" memories. J. Neurosci. 2011;31(22):8175-8180.