Serotonin selectively enhances perception and sensory neural responses to stimuli generated by same-sex conspecifics

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

Volumn 110, Issue 48, 2013, Pages 19609-19614

  Deemyad, Tara ^a,b   Metzen, Michael G ^a   Pan, Yingzhou ^a   Chacron, Maurice J ^a  

^a MCGILL UNIVERSITY   (Canada)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Excitability; Neural coding; Neuroethology; Neuromodulation

Indexed keywords

SEROTONIN;

AFTERHYPERPOLARIZATION; AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; ELECTRIC FISH; ELECTROSTIMULATION; FEMALE; INNERVATION; MALE; NERVE CELL STIMULATION; NERVE CONDUCTION; NERVE EXCITABILITY; NERVE POTENTIAL; NONHUMAN; PERCEPTION; PREY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SENSORY NERVE; SEROTONINERGIC SYSTEM; SPIKE; STIMULUS RESPONSE;

EXCITABILITY; NEURAL CODING; NEUROETHOLOGY; NEUROMODULATION;

ACTION POTENTIALS; ANIMALS; ELECTRIC STIMULATION; FEMALE; GYMNOTIFORMES; MALE; PYRAMIDAL CELLS; SENSORY RECEPTOR CELLS; SEROTONIN; SOCIAL DOMINANCE; SYNAPTIC TRANSMISSION;

EID: 84888325941     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1314008110     Document Type: Article

References (42)

1. Wark B, Lundstrom BN, Fairhall A (2007) Sensory adaptation. Curr Opin Neurobiol 17(4): 423-429.
2. Marder E (2012) Neuromodulation of neuronal circuits: Back to the future. Neuron 76(1): 1-11.
3. Hurley LM, Devilbiss DM, Waterhouse BD (2004) A matter of focus: Monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr Opin Neurobiol 14(4): 488-495.
4. Foehring RC, van Brederode JF, Kinney GA, Spain WJ (2002) Serotonergic modulation of supragranular neurons in rat sensorimotor cortex. J Neurosci 22(18): 8238-8250.
5. Thompson AM, Hurley LM (2004) Dense serotonergic innervation of principal nuclei of the superior olivary complex in mouse. Neurosci Lett 356(3): 179-182.
6. Petzold GC, Hagiwara A, Murthy VN (2009) Serotonergic modulation of odor input to the mammalian olfactory bulb. Nat Neurosci 12(6): 784-791.
7. Hurley LM, Pollak GD (2005) Serotonin shifts first-spike latencies of inferior colliculus neurons. J Neurosci 25(34): 7876-7886.
8. Chacron MJ, Longtin A, Maler L (2011) Efficient computation via sparse coding in electrosensory neural networks. Curr Opin Neurobiol 21(5): 752-760.
9. Nelson ME, Maciver MA (1999) Prey capture in the weakly electric fish Apteronotus albifrons: Sensory acquisition strategies and electrosensory consequences. J Exp Biol 202(Pt 10): 1195-1203.
10. Zakon HH, Oestreich J, Tallarovic S, Triefenbach F (2002) EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips. J Physiol Paris 96(5-6): 451-458.
11. Deemyad T, Maler L, Chacron MJ (2011) Inhibition of SK and M channel-mediated currents by 5-HT enables parallel processing by bursts and isolated spikes. J Neurophysiol 105(3): 1276-1294.
12. Márquez BT, Krahe R, Chacron MJ (2013) Neuromodulation of early electrosensory processing in gymnotiform weakly electric fish. J Exp Biol 216(Pt 13): 2442-2450.
13. Toporikova N, Chacron MJ (2009) SK channels gate information processing in vivo by regulating an intrinsic bursting mechanism seen in vitro. J Neurophysiol 102(4): 2273-2287.
14. Heiligenberg W (1991) Neural Nets in Electric Fish (MIT Press, Cambridge, MA).
15. Hitschfeld ÉM, Stamper SA, Vonderschen K, Fortune ES, Chacron MJ (2009) Effects of restraint and immobilization on electrosensory behaviors of weakly electric fish. ILAR J 50(4): 361-372.
16. Carlson BA, Kawasaki M (2006) Ambiguous encoding of stimuli by primary sensory afferents causes a lack of independence in the perception of multiple stimulus attributes. J Neurosci 26(36): 9173-9183.
17. Smith GT, Combs N (2008) Serotonergic activation of 5HT1A and 5HT2 receptors modulates sexually dimorphic communication signals in the weakly electric fish Apteronotus leptorhynchus. Horm Behav 54(1): 69-82.
18. Lemon N, Turner RW (2000) Conditional spike backpropagation generates burst discharge in a sensory neuron. J Neurophysiol 84(3): 1519-1530.
19. Mehaffey WH, Doiron B, Maler L, Turner RW (2005) Deterministic multiplicative gain control with active dendrites. J Neurosci 25(43): 9968-9977.
20. Bastian J, Nguyenkim J (2001) Dendritic modulation of burst-like firing in sensory neurons. J Neurophysiol 85(1): 10-22.
21. Marsat G, Proville RD, Maler L (2009) Transient signals trigger synchronous bursts in an identified population of neurons. J Neurophysiol 102(2): 714-723.
22. Oswald AMM, Chacron MJ, Doiron B, Bastian J, Maler L (2004) Parallel processing of sensory input by bursts and isolated spikes. J Neurosci 24(18): 4351-4362.
23. Berman NJ, Maler L (1999) Neural architecture of the electrosensory lateral line lobe: Adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. J Exp Biol 202(Pt 10): 1243-1253.
24. Bastian J, Chacron MJ, Maler L (2004) Plastic and nonplastic pyramidal cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron 41(5): 767-779.
25. Chacron MJ, Maler L, Bastian J (2005) Feedback and feedforward control of frequency tuning to naturalistic stimuli. J Neurosci 25(23): 5521-5532.
26. Bol K, Marsat G, Harvey-Girard E, Longtin A, Maler L (2011) Frequency-tuned cerebellar channels and burst-induced LTD lead to the cancellation of redundant sensory inputs. J Neurosci 31(30): 11028-11038.
27. Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 5(1): 13-23.
28. Lesica NA, Stanley GB (2004) Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus. J Neurosci 24(47): 10731-10740.
29. Ellis LD, Maler L, Dunn RJ (2008) Differential distribution of SK channel subtypes in the brain of the weakly electric fish Apteronotus leptorhynchus. J Comp Neurol 507(6): 1964-1978.
30. Stefani A, Surmeier DJ, Kitai ST (1990) Serotonin enhances excitability in neostriatal neurons by reducing voltage-dependent potassium currents. Brain Res 529(1-2): 354-357.
31. Massaux A, Dutrieux G, Cotillon-Williams N, Manunta Y, Edeline JM (2004) Auditory thalamus bursts in anesthetized and non-anesthetized states: Contribution to functional properties. J Neurophysiol 91(5): 2117-2134.
32. Johnston SA, Maler L, Tinner B (1990) The distribution of serotonin in the brain of Apteronotus leptorhynchus: an immunohistochemical study. J Chem Neuroanat 3(6): 429-465.
33. Vonderschen K, Chacron MJ (2011) Sparse and dense coding of natural stimuli by distinct midbrain neuron subpopulations in weakly electric fish. J Neurophysiol 106(6): 3102-3118.
34. Montoya ER, Terburg D, Bos PA, van Honk J (2012) Testosterone, cortisol, and serotonin as key regulators of social aggression: A review and theoretical perspective. Motiv Emot 36(1): 65-73.
35. Fachinelli C, Sargo S, Bataller R, Rodríguez Echandía EL (1989) Effect of 5-HTP and ketanserine on the aggressive reaction induced by food competition in dominant and submissive pigeons (Columba livia). Behav Brain Res 35(3): 265-270.
36. Tops M, Russo S, Boksem MA, Tucker DM (2009) Serotonin: Modulator of a drive to withdraw. Brain Cogn 71(3): 427-436.
37. Larson ET, Summers CH (2001) Serotonin reverses dominant social status. Behav Brain Res 121(1-2): 95-102.
38. Parent A (1981) Comparative anatomy of the serotoninergic systems. J Physiol (Paris) 77(2-3): 147-156.
39. Bastian J (1993) The role of amino acid neurotransmitters in the descending control of electroreception. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 172(4): 409-423.
40. Bastian J, Chacron MJ, Maler L (2002) Receptive field organization determines pyramidal cell stimulus-encoding capability and spatial stimulus selectivity. J Neurosci 22(11): 4577-4590.
41. Harrington JK, et al. (2011) Determining the fate of seeded cells in venous tissueengineered vascular grafts using serial MRI. FASEB J 25(12): 4150-4161.
42. Faber ESL, Sah P (2002) Physiological role of calcium-activated potassium currents in the rat lateral amygdala. J Neurosci 22(5): 1618-1628.