Plasticity during motherhood: Changes in excitatory and inhibitory layer 2/3 neurons in auditory cortex

Journal of Neuroscience

Volumn 35, Issue 4, 2015, Pages 1806-1815

  Cohen, Lior ^a   Mizrahi, Adi ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Feed forward inhibition; Motherhood; Pup odors; Ultrasonic vocalizations

Indexed keywords

PARVALBUMIN; GLUTAMIC ACID; PLANT LECTIN; TOMATO LECTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; BRAIN ELECTROPHYSIOLOGY; CELL ACTIVITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EVOKED RESPONSE; EXCITATORY NEURON; FEMALE; FLUORESCENCE MICROSCOPY; FREQUENCY ANALYSIS; IMMUNOHISTOCHEMISTRY; INHIBITORY NEURON; LACTATION; MATERNAL BEHAVIOR; MOTHER; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; ODOR; OLFACTORY NERVE; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL GLUTAMATERGIC NEURON; SPIKE WAVE; ULTRASONIC VOCALIZATION; VOCALIZATION; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENETICS; MEMBRANE POTENTIAL; METABOLISM; NERVE CELL INHIBITION; NEWBORN; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; PROCEDURES; TRANSGENIC MOUSE;

ACOUSTIC STIMULATION; ANIMALS; ANIMALS, NEWBORN; AUDITORY CORTEX; FEMALE; GLUTAMIC ACID; MATERNAL BEHAVIOR; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONAL PLASTICITY; NEURONS; ODORS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; PLANT LECTINS;

EID: 84921925229     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1786-14.2015     Document Type: Article

References (58)

1. Bertram R, Helena CV, Gonzalez-Iglesias AE, Tabak J, Freeman ME (2010) A tale of two rhythms: the emerging roles of oxytocin in rhythmic prolactin release. J Neuroendocrinol 22:778-784. CrossRef Medline
2. Brudzynski SM (2009) Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J 50:43-50. CrossRef Medline
3. Brunton PJ, Russell JA (2008) The expectant brain: adapting for motherhood. Nat Rev Neurosci 9:11-25. CrossRef Medline
4. Carcea I, Froemke RC (2013) Cortical plasticity, excitatory-inhibitory balance, and sensory perception. Prog Brain Res 207:65-90. CrossRef Medline
5. Chase SM, Young ED (2007) First-spike latency information in single neurons increases when referenced to population onset. Proc Natl Acad Sci U S A 104:5175-5180. CrossRef Medline
6. Cohen L, Rothschild G, Mizrahi A (2011) Multisensory integration of natural odors and sounds in the auditory cortex. Neuron 72:357-369. CrossRef Medline
7. Cohen L, Koffman N, Meiri H, Yarom Y, Lampl I, Mizrahi A (2013) Timelapse electrical recordings of single neurons from the mouse neocortex. Proc Natl Acad Sci U S A 110:5665-5670. CrossRef Medline
8. Dulac C, O’Connell LA, Wu Z (2014) Neural control of maternal and paternal behaviors. Science 345:765-770. CrossRef Medline
9. Ehret G (2005) Infant rodent ultrasounds—a gate to the understanding of sound communication. Behav Genet 35:19-29. CrossRef Medline
10. Ferguson JN, Aldag JM, Insel TR, Young LJ (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neurosci 21: 8278-8285. Medline
11. Fino E, Packer AM, Yuste R (2013) The logic of inhibitory connectivity in the neocortex. Neuroscientist 19:228-237. CrossRef Medline
12. Francis DD, Champagne FC, Meaney MJ (2000) Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12:1145-1148. CrossRef Medline
13. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56:33-42. CrossRef Medline
14. Galindo-Leon EE, Lin FG, Liu RC (2009) Inhibitory plasticity in a lateral band improves cortical detection of natural vocalizations. Neuron 62: 705-716. CrossRef Medline
15. Hahn ME, Lavooy MJ (2005) A review of the methods of studies on infant ultrasound production and maternal retrieval in small rodents. Behav Genet 35:31-52. CrossRef Medline
16. Happel MF, Jeschke M, Ohl FW (2010) Spectral integration in primary auditory cortex attributable to temporally precise convergence of thalamocortical and intracortical input. J Neurosci 30:11114-11127. CrossRef Medline
17. Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, Ladle DR, Arber S (2005) A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3:e159. CrossRef Medline
18. Judkewitz B, Rizzi M, Kitamura K, Häusser M (2009) Targeted single-cell electroporation of mammalian neurons in vivo. Nat Protoc 4:862-869. CrossRef Medline
19. Kitamura K, Judkewitz B, Kano M, Denk W, Häusser M (2008) Targeted patch-clamp recordings and single-cell electroporation of unlabeled neurons in vivo. Nat Methods 5:61-67. CrossRef Medline
20. Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J, Herry C, Lüthi A (2011) A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480:331-335. CrossRef Medline
21. Leuner B, Glasper ER, Gould E (2010) Parenting and plasticity. Trends Neurosci 33:465-473. CrossRef Medline
22. Lévy F, Keller M (2009) Olfactory mediation of maternal behavior in selected mammalian species. Behav Brain Res 200:336-345. CrossRef Medline
23. Lévy F, Keller M, Poindron P (2004) Olfactory regulation of maternal behavior in mammals. Horm Behav 46:284-302. CrossRef Medline
24. Liu BH, Wu GK, Arbuckle R, Tao HW, Zhang LI (2007) Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci 10: 1594-1600. CrossRef Medline
25. Liu RC, Schreiner CE (2007) Auditory cortical detection and discrimination correlates with communicative significance. PLoS Biol 5:e173. CrossRef Medline
26. Liu RC, Linden JF, Schreiner CE (2006) Improved cortical entrainment to infant communication calls in mothers compared with virgin mice. Eur J Neurosci 23:3087-3097. CrossRef Medline
27. Lundström JN, Mathe A, Schaal B, Frasnelli J, Nitzsche K, Gerber J, Hummel T (2013) Maternal status regulates cortical responses to the body odor of newborns. Front Psychol 4:597. CrossRef Medline
28. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133-140. CrossRef Medline
29. Margrie TW, Meyer AH, Caputi A, Monyer H, Hasan MT, Schaefer AT, Denk W, Brecht M (2003) Targeted whole-cell recordings in the mammalian brain in vivo. Neuron 39:911-918. CrossRef Medline
30. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807. CrossRef Medline
31. Moore AK, Wehr M (2013) Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J Neurosci 33: 13713-13723. CrossRef Medline
32. Noirot E (1972) Ultrasounds and maternal behavior in small rodents. Dev Psychobiol 5:371-387. CrossRef Medline
33. O’Connell MN, Falchier A, McGinnis T, Schroeder CE, Lakatos P (2011) Dual mechanism of neuronal ensemble inhibition in primary auditory cortex. Neuron 69:805-817. CrossRef Medline
34. Okabe S, Nagasawa M, Kihara T, Kato M, Harada T, Koshida N, Mogi K, Kikusui T (2013) Pup odor and ultrasonic vocalizations synergistically stimulate maternal attention in mice. Behav Neurosci 127:432-438. CrossRef Medline
35. Okun M, Lampl I (2008) Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat Neurosci 11: 535-537. CrossRef Medline
36. Oswald AM, Reyes AD (2011) Development of inhibitory timescales in auditory cortex. Cereb Cortex 21:1351-1361. CrossRef Medline
37. Pedersen CA, Vadlamudi SV, Boccia ML, Amico JA (2006) Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes Brain Behav 5:274-281. CrossRef Medline
38. Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M (2013) Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci 16:1068-1076. CrossRef Medline
39. Pi HJ, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A (2013) Cortical interneurons that specialize in disinhibitory control. Nature 503: 521-524. CrossRef Medline
40. Rilling JK, Young LJ (2014) The biology of mammalian parenting and its effect on offspring social development. Science 345:771-776. CrossRef Medline
41. Ross HE, Young LJ (2009) Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrinol 30:534-547. CrossRef Medline
42. Rothschild G, Nelken I, Mizrahi A (2010) Functional organization and population dynamics in the mouse primary auditory cortex. Nat Neurosci 13:353-360. CrossRef Medline
43. Rothschild G, Cohen L, Mizrahi A, Nelken I (2013) Elevated correlations in neuronal ensembles of mouse auditory cortex following parturition. J Neurosci 33:12851-12861. CrossRef Medline
44. Scattoni ML, Crawley J, Ricceri L (2009) Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci Biobehav Rev 33:508-515. CrossRef Medline
45. Schreiner CE, Polley DB (2014) Auditory map plasticity: diversity in causes and consequences. Curr Opin Neurobiol 24:143-156. CrossRef Medline
46. Sewell GD (1970) Ultrasonic communication in rodents. Nature 227:410. CrossRef Medline
47. Shughrue PJ, Dellovade TL, Merchenthaler I (2002) Estrogen modulates oxytocin gene expression in regions of the rat supraoptic and paraventricular nuclei that contain estrogen receptor-beta. Prog Brain Res 139: 15-29. CrossRef Medline
48. Smotherman WP, Bell RW, Starzec J, Elias J, Zachman TA (1974) Maternal responses to infant vocalizations and olfactory cues in rats and mice. Behav Biol 12:55-66. CrossRef Medline
49. Stiebler I, Neulist R, Fichtel I, Ehret G (1997) The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 181:559-571. CrossRef Medline
50. Stoop R (2012) Neuromodulation by oxytocin and vasopressin. Neuron 76: 142-159. CrossRef Medline
51. Swain JE, Kim P, Ho SS (2011) Neuroendocrinology of parental response to baby-cry. J Neuroendocrinol 23:1036-1041. CrossRef Medline
52. Tan AY, Wehr M (2009) Balanced tone-evoked synaptic excitation and inhibition in mouse auditory cortex. Neuroscience 163:1302-1315. CrossRef Medline
53. Tao HW, Li YT, Zhang LI (2014) Formation of excitation-inhibition balance: inhibition listens and changes its tune. Trends Neurosci 37:528-530. CrossRef Medline
54. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446. CrossRef Medline
55. Wu GK, Arbuckle R, Liu BH, Tao HW, Zhang LI (2008) Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 58:132-143. CrossRef Medline
56. Xu X, Roby KD, Callaway EM (2010) Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 518:389-404. CrossRef Medline
57. Yazaki-Sugiyama Y, Kang S, Câteau H, Fukai T, Hensch TK (2009) Bidirectional plasticity in fast-spikingGABAcircuits by visual experience. Nature 462:218-221. CrossRef Medline
58. Zhou Y, Mesik L, Sun YJ, Liang F, Xiao Z, Tao HW, Zhang LI (2012) Generation of spike latency tuning by thalamocortical circuits in auditory cortex. J Neurosci 32:9969-9980. CrossRef Medline