Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 49, 2015, Pages 15208-15213

  Veit, Lena ^a   Pidpruzhnykova, Galyna ^a,b   Nieder, Andreas ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b EPFL   (Switzerland)

Author keywords

Association learning; Crow; Memory; Nidopallium caudolaterale; Single cell recordings

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BEHAVIOR; BRAIN FUNCTION; BRAIN NERVE CELL; CONTROLLED STUDY; CORVUS; CORVUS CORONE; CROW; NIDOPALLIUM CAUDOLATERALE; NONHUMAN; PRIORITY JOURNAL; STATE DEPENDENT LEARNING; TASK PERFORMANCE; TELENCEPHALON; ANIMAL; ANIMAL BEHAVIOR; LEARNING; NERVE CELL; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; CROWS; LEARNING; NEURONS;

EID: 84949239033     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1509760112     Document Type: Article

References (40)

1. Emery NJ, Clayton NS (2004) The mentality of crows: Convergent evolution of intelligence in corvids and apes. Science 306(5703):1903-1907.
2. Nishizawa K, Izawa EI, Watanabe S (2011) Neural-activity mapping of memory-based dominance in the crow: neural networks integrating individual discrimination and social behaviour control. Neuroscience 197:307-319.
3. Clayton NS, Yu KS, Dickinson A (2001) Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes. J Exp Psychol Anim Behav Process 27(1):17-29.
4. Veit L, Nieder A (2013) Abstract rule neurons in the endbrain support intelligent behaviour in corvid songbirds. Nat Commun 4:2878.
5. Hartmann B, Güntürkün O (1998) Selective deficits in reversal learning after neostriatum caudolaterale lesions in pigeons: Possible behavioral equivalencies to the mammalian prefrontal system. Behav Brain Res 96(1-2):125-133.
6. Güntürkün O (2005) The avian 'prefrontal cortex' and cognition. Curr Opin Neurobiol 15(6):686-693.
7. Puig MV, Rose J, Schmidt R, Freund N (2014) Dopamine modulation of learning and memory in the prefrontal cortex: Insights from studies in primates, rodents, and birds. Front Neural Circuits 8:93.
8. Smith AC, Wirth S, Suzuki WA, Brown EN (2007) Bayesian analysis of interleaved learning and response bias in behavioral experiments. J Neurophysiol 97(3): 2516-2524.
9. Veit L, Hartmann K, Nieder A (2014) Neuronal correlates of visual working memory in the corvid endbrain. J Neurosci 34(23):7778-7786.
10. Ditz HM, Nieder A (2015) Neurons selective to the number of visual items in the corvid songbird endbrain. Proc Natl Acad Sci USA 112(25):7827-7832.
11. Roitblat HL (1980) Codes and coding processes in pigeon short-term memory. Anim Learn Behav8(3):341-351.
12. Gaffan D (1977) Response coding in recall of colours by monkeys. Q J Exp Psychol 29(4):597-605.
13. Rainer G, Rao SC, Miller EK (1999) Prospective coding for objects in primate prefrontal cortex. J Neurosci 19(13):5493-5505.
14. Asaad WF, Rainer G, Miller EK (1998) Neural activity in the primate prefrontal cortex during associative learning. Neuron 21(6):1399-1407.
15. Cromer JA, Machon M, Miller EK (2011) Rapid association learning in the primate prefrontal cortex in the absence of behavioral reversals. J Cogn Neurosci 23(7): 1823-1828.
16. Pasupathy A, Miller EK (2005) Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature 433(7028):873-876.
17. Brincat SL, Miller EK (2015) Frequency-specific hippocampal-prefrontal interactions during associative learning. Nat Neurosci 18(4):576-581.
18. Freedman DJ, Riesenhuber M, Poggio T, Miller EK (2002) Visual categorization and the primate prefrontal cortex: Neurophysiology and behavior. J Neurophysiol 88(2): 929-941.
19. Tomita H, Ohbayashi M, Nakahara K, Hasegawa I, Miyashita Y (1999) Top-down signal from prefrontal cortex in executive control of memory retrieval. Nature 401(6754): 699-703.
20. Nieder A (2012) Supramodal numerosity selectivity of neurons in primate prefrontal and posterior parietal cortices. Proc Natl Acad Sci USA 109(29):11860-11865.
21. Hirabayashi T, Takeuchi D, Tamura K, Miyashita Y (2013) Functional microcircuit recruited during retrieval of object association memory in monkey perirhinal cortex. Neuron 77(1):192-203.
22. Hirabayashi T, Miyashita Y (2014) Computational principles of microcircuits for visual object processing in the macaque temporal cortex. Trends Neurosci 37(3):178-187.
23. Gentner TQ, Margoliash D (2003) Neuronal populations and single cells representing learned auditory objects. Nature 424(6949):669-674.
24. Jeanne JM, Thompson JV, Sharpee TO, Gentner TQ (2011) Emergence of learned categorical representations within an auditory forebrain circuit. J Neurosci 31(7): 2595-2606.
25. Jeanne JM, Sharpee TO, Gentner TQ (2013) Associative learning enhances population coding by inverting interneuronal correlation patterns. Neuron 78(2):352-363.
26. Kröner S, Güntürkün O (1999) Afferent and efferent connections of the caudolateral neostriatum in the pigeon (Columba livia): A retro-and anterograde pathway tracing study. J Comp Neurol 407(2):228-260.
27. Wirth S, et al. (2003) Single neurons in the monkey hippocampus and learning of new associations. Science 300(5625):1578-1581.
28. Wirth S, et al. (2009) Trial outcome and associative learning signals in the monkey hippocampus. Neuron 61(6):930-940.
29. Yanike M, Wirth S, Smith AC, Brown EN, Suzuki WA (2009) Comparison of associative learning-related signals in the macaque perirhinal cortex and hippocampus. Cereb Cortex 19(5):1064-1078.
30. Suzuki WA, Brown EN (2005) Behavioral and neurophysiological analyses of dynamic learning processes. Behav Cogn Neurosci Rev 4(2):67-95.
31. Benchenane K, et al. (2010) Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 66(6):921-936.
32. Rattenborg NC, Martinez-Gonzalez D (2011) A bird-brain view of episodic memory. Behav Brain Res 222(1):236-245.
33. Atoji Y, Wild JM, Yamamoto Y, Suzuki Y (2002) Intratelencephalic connections of the hippocampus in pigeons (Columba livia). J Comp Neurol 447(2):177-199.
34. Chen LL, Wise SP (1995) Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. J Neurophysiol 73(3):1101-1121.
35. Chen LL, Wise SP (1995) Supplementary eye field contrasted with the frontal eye field during acquisition of conditional oculomotor associations. J Neurophysiol 73(3): 1122-1134.
36. Rainer G, Miller EK (2000) Effects of visual experience on the representation of objects in the prefrontal cortex. Neuron 27(1):179-189.
37. Puig MV, Miller EK (2012) The role of prefrontal dopamine D1 receptors in the neural mechanisms of associative learning. Neuron 74(5):874-886.
38. Moll FW, Nieder A (2015) Cross-modal associative mnemonic signals in crow endbrain neurons. Curr Biol 25(16):2196-2201.
39. Hoffmann A, Rüttler V, Nieder A (2011) Ontogeny of object permanence and object tracking in the carrion crow, Corvus corone. Anim Behav 82:359-367.
40. Green DM, Swets JA (1966) Signal Detection Theory and Psychophysics (Wiley, New York).