Somatosensory control of the onset and retention of maternal responsiveness in primiparous Sprague–Dawley rats
Abstract
The role of perioral and ventral-trunk somatosensory stimulation from pups mediating the initial expression of maternal behavior and its long-term retention 8 days later, was investigated. Six groups of female rats were permitted to physically interact with four 1-5-day-old foster pups for 1 h, 36 h after Cesarean delivery on gestation day 21. Prior to this maternal experience, dams were subjected to: reduced cutaneous rostral snout sensitivity (anaptia) by injection of lidocaine into the mystacial pads; reduced ventral-trunk sensations by occlusion of the entire ventrum with a full spandex jacket; both manipulations; or control manipulations. Additional groups of females not receiving a maternal experience (inexperienced) also received the somatosensory deprivation or control manipulations. During retention testing, rats in the singly manipulated experienced groups exhibited reduced latencies to become maternal in comparison to their inexperienced counterparts (approximately 3 days vs. 8 days). However, rats previously rendered both anaptic and ventrally-occluded responded like inexperienced rats in showing a long latency to become maternal (8 days). Thus, reduction of either perioral or ventral somatosensory contact from pups did not block the maternal experience effect, but reduction of both of these inputs did.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Vaginal delivery provides critical sensory stimulation that increases release of OT and helps to establish maternal behaviors.
“Vaginal delivery provides critical sensory stimulation that increases release of OT and helps to establish maternal behaviors (Morgan et al., 1992).”
From The maternal brain and its plasticity in humans (2016) · cites this paper as Morgan et al., 1992
Cites
Rheingold, H. L. (1963) · Medical Entomology and Zoology · Cited by 886 · see citing works
Nonhormonal basis of maternal behavior in the rat
Rosenblatt, J. S. (1967) · Science · doi:10.1126/science.156.3781.1512 · Cited by 721 · see citing works
Stern, J. M., & Johnson, S. K. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90026-z · Cited by 301 · see citing works
Self-citationFleming, A. S., & Rosenblatt, J. S. (1974) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0035937 · Cited by 257 · see citing works
Self-citationNMDA receptor activation and early olfactory learning
Lincoln, J., Coopersmith, R., Harris, E. W., Cotman, C. W., & Leon, M. (1988) · Developmental Brain Research · doi:10.1016/0165-3806(88)90036-3 · Cited by 221 · see citing works
Beach, F. A., & Jaynes, J. (1956) · Behaviour · doi:10.1163/156853956x00129 · Cited by 192 · see citing works
Long-term effects of pregnancy and parturition upon maternal responsiveness in the rat
Bridges, R. S. (1975) · Physiology & Behavior · doi:10.1016/0031-9384(75)90028-1 · Cited by 189 · see citing works
Experience with pups sustains maternal responding in postpartum rats
Orpen, B. G., & Fleming, A. S. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90184-3 · Cited by 159 · see citing works
Self-citationEarly olfactory learning induces an enhanced olfactory bulb response in young rats
Sullivan, R. M., & Leon, M. (1986) · Developmental Brain Research · doi:10.1016/0165-3806(86)90256-7 · Cited by 151 · see citing works
Stone, C. P., Wiesner, B. P., & Sheard, N. M. (1934) · The American Journal of Psychology · doi:10.2307/1416582 · Cited by 133 · see citing works
Maternal Behavior: Sensory, Hormonal, and Neural Determinants
Stern, J. M. (1989) · Elsevier eBooks · doi:10.1016/b978-0-12-137952-0.50008-2 · Cited by 131 · see citing works
Self-citationEndocrine regulation of parental behavior in rodents.
Bridges, R. S. (1990) · Cited by 115 · see citing works
Prepartum changes in maternal responsiveness and nest defense in Rattus norvegicus.
Mayer, A. D., & Rosenblatt, J. S. (1984) · Journal of comparative psychology · doi:10.1037/0735-7036.98.2.177 · Cited by 112 · see citing works
Parturition: Its role in the long term retention of maternal behavior in the rat☆☆☆
Bridges, R. S. (1977) · Physiology & Behavior · doi:10.1016/0031-9384(77)90263-3 · Cited by 106 · see citing works
Aspects of nonhormonal maternal behavior in the rat*1
Terkel, J. (1971) · Hormones and Behavior · doi:10.1016/0018-506x(71)90031-6 · Cited by 95 · see citing works
Perioral somatosensory determinants of nursing behavior in Norway rats (Rattus norvegicus).
Stern, J. M., & Johnson, S. K. (1989) · Journal of comparative psychology · doi:10.1037/0735-7036.103.3.269 · Cited by 90 · see citing works
Self-citationMultisensory regulation of maternal behavior and masculine sexual behavior: A revised view
Stern, J. M. (1990) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80219-2 · Cited by 86 · see citing works
Self-citationCohen, J. A., & Bridges, R. S. (1981) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077781 · Cited by 86 · see citing works
Enhanced neural response by adult rats to odors experienced early in life
Coopersmith, R., & Leon, M. (1986) · Brain Research · doi:10.1016/0006-8993(86)90384-7 · Cited by 76 · see citing works
Initiation of maternal behavior in pregnant nulliparous rats
Slotnick, B. M., Carpenter, M. L., & Fusco, R. (1973) · Hormones and Behavior · doi:10.1016/0018-506x(73)90016-0 · Cited by 74 · see citing works
Exteroceptive stimulation of maternal behavior in the naive rat
Herrenkohl, L. R., & Rosenberg, P. A. (1972) · Physiology & Behavior · doi:10.1016/0031-9384(72)90080-7 · Cited by 72 · see citing works
Experience-hormone interactions and maternal behavior in rats
Fleming, A. S., & Sarker, J. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90368-e · Cited by 70 · see citing works
Self-citationPerioral anesthesia disrupts maternal behavior during early lactation in long—evans rats
Stern, J. M., & Kolunie, J. M. (1989) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(89)90134-9 · Cited by 66 · see citing works
Self-citationSTERN, J. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90271-8 · Cited by 55 · see citing works
Self-citationStudies on Maternal Retrieving in Rats: II. Effects of Practice and Previous Parturitions
Beach, F. A., & Jaynes, J. (1956) · The American Naturalist · doi:10.1086/281913 · Cited by 53 · see citing works
Hormonal influences on the duration of postpartum maternal responsiveness in the rat
Orpen, B. G., Furman, N., Wong, P. Y., & Fleming, A. S. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90052-7 · Cited by 53 · see citing works
Self-citationEstablishment and maintenance of maternal responsiveness in postpartum Wistar rats
Jakubowski, M., & Terkel, J. (1986) · Animal Behaviour · doi:10.1016/0003-3472(86)90030-8 · Cited by 46 · see citing works
Neurokinetics of Lidocaine in the Infraorbital Nerve of the Rat in Vivo
Fink, B. R., Aasheim, G. M., Kish, S. J., & Croley, T. S. (1975) · Anesthesiology · doi:10.1097/00000542-197506000-00017 · Cited by 45 · see citing works
Malenfant, S. A., Barry, M., & Fleming, A. S. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90045-p · Cited by 41 · see citing works
Self-citationRole of the infraorbital nerve in retrieving behavior in lactating rats.
Kenyon, P. R., Cronin, P., & Keeble, S. (1983) · Behavioral Neuroscience · doi:10.1037//0735-7044.97.2.255 · Cited by 39 · see citing works
Disruption of maternal retrieving by perioral anesthesia
Kenyon, P. R., Cronin, P., & Keeble, S. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90274-2 · Cited by 39 · see citing works
Malenfant, S. A., O'Hearn, S., & Fleming, A. S. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90340-t · Cited by 34 · see citing works
Self-citationRole of the infraorbital nerve in retrieving behavior in lactating rats.
Kenyon, P. R., Cronin, P., & Keeble, S. (1983) · Behavioral Neuroscience · doi:10.1037/0735-7044.97.2.255 · Cited by 31 · see citing works
Stern, J. M. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90167-2 · Cited by 22 · see citing works
Self-citation
Flagged first, then by citations
2 of the 36 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
“Despite the display of maternal behavior, without tactile sensation either on the ventrum or the snout, conditioned place preference, which involves the pairing of context with reward, does not develop as a result of exposure to pups (Fleming et al. 1994; Morgan et al. 1992; Stern 1990).”
BackgroundFleming, A. S., O’Day, D. H., & Kraemer, G. W. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00011-1 · Cited by 429 · see citing works
“If new mothers are rendered anosmic and cannot smell pups and are also unable to acquire somatosensory stimulation of the ventrum and mouth regions (due to application of anesthetic onto or into these regions), pups are not licked or retrieved [37,38].”
Self-citationNeuroendocrine regulation of maternal behavior
Bridges, R. S. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.11.007 · Cited by 346 · see citing works
The maternal brain and its plasticity in humans
Kim, P., Strathearn, L., & Swain, J. E. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.08.001 · Cited by 278 · see citing works
“Vaginal delivery provides critical sensory stimulation that increases release of OT andhelps to establishmaternal behaviors (Morgan et al., 1992).”
Regulation of anxiety during the postpartum period
Lonstein, J. S. (2007) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2007.05.002 · Cited by 229 · see citing works
“Rooting in their dam’s ventrum while searching for a nipple does have physiological consequences for the mother [269,270,310,408], but perioral stimulation that dams receive during interactions with pups may also be sufficient to reduce anxiety [315].”
BackgroundMaternal brain response to own baby‐cry is affected by cesarean section delivery
Swain, J. E., Tasgin, E., Mayes, L. C., Feldman, R., Todd Constable, R., & Leckman, J. F. (2008) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2008.01963.x · Cited by 206 · see citing works
Oxytocin and mutual communication in mother-infant bonding
Nagasawa, M., Okabe, S., Mogi, K., & Kikusui, T. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00031 · Cited by 202 · see citing works
“Similarly, removal of the vomeronasal organ, such as vomeronasal nerve cuts or olfactory bulbectomy, did not fully disrupt maternal behavior (Jirik-Babb et al., 1984; Morgan et al., 1992).”
BackgroundFleming, A. S., Korsmit, M., & Deller, M. (1994) · Psychobiology · doi:10.3758/bf03327079 · Cited by 186 · see citing works
Self-citationSomatosensation and Maternal Care in Norway Rats
Stern, J. M. (1996) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60335-6 · Cited by 181 · see citing works
Self-citationOxytocin Control of Maternal Behavior Regulation by Sex Steroids and Offspring Stimuli<sup>a</sup>
PEDERSEN, C. A. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51916.x · Cited by 172 · see citing works
Alterations of the cortical representation of the rat ventrum induced by nursing behavior
Xerri, C., Stern, J. M., & Merzenich, M. M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-03-01710.1994 · Cited by 167 · see citing works
“Changes in SI probably also occur in the zone of representation of the snout and vibrissae, inputs from which have also been demonstrated to be important for aspects of maternal behavior (Kenyon et al., 1981, 1983; Stern and Kolunie, 1989, 1991; Morgan et al., 1992).”
BackgroundSelf-citationLimbic system fos expression associated with paternal behavior
Kirkpatrick, B. W., Kim, J. W., & Insel, T. R. (1994) · Brain Research · doi:10.1016/s0006-8993(09)90016-6 · Cited by 165 · see citing works
Complete maternal deprivation affects social, but not spatial, learning in adult rats
Lévy, F., Melo, Á. I., Galef, B. G., Madden, M., & Fleming, A. S. (2003) · Developmental Psychobiology · doi:10.1002/dev.10131 · Cited by 161 · see citing works
Self-citationLonstein, J. S., Lévy, F., & Fleming, A. S. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.06.011 · Cited by 151 · see citing works
“disrupts the onset of maternal behavior at parturition (Stern, 1996b), and when infraorbital anesthesia is combined with ventral anesthesia, maintenance of maternal responsiveness beyond parturition is prevented (Morgan et al., 1992).”
InfluentialSelf-citationLonstein, J. S. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.11.001 · Cited by 147 · see citing works
Fleming, A. S., & Korsmit, M. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.3.567 · Cited by 136 · see citing works
Self-citationEffects of stress during pregnancy on maternal behavior in mice
Meek, L. R., Dittel, P. L., Sheehan, M. C., Chan, J. Y., & Kjolhaug, S. R. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00431-5 · Cited by 122 · see citing works
Oxytocin Links Mothering Received, Mothering Bestowed and Adult Stress Responses
Pedersen, C. A., & Boccia, M. L. (2002) · Stress · doi:10.1080/1025389021000037586 · Cited by 116 · see citing works
“Therefore, it is unlikely that OTA indirectly influenced PL–ABN by altering pup behavior (Morgan et al., 1992; Stern, 1996).”
BackgroundGonzález‐Mariscal, G., & Poindron, P. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50005-6 · Cited by 115 · see citing works
Pereira, M., & Morrell, J. I. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.06.026 · Cited by 107 · see citing works
Neuropsychology of maternal behavior in the rat: c-fos expression during mother-litter interactions
Fleming, A. S., & Walsh, C. J. (1994) · Psychoneuroendocrinology · doi:10.1016/0306-4530(94)90030-2 · Cited by 101 · see citing works
Self-citationJohns, J. M., Noonan, L. R., Zimmerman, L. I., Li, L., & al, E. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.1.107 · Cited by 100 · see citing works
Walsh, C. J., Fleming, A. S., Lee, A., & Magnusson, J. E. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.1.134 · Cited by 96 · see citing works
Self-citationPereira, M., & Ferreira, A. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.08.013 · Cited by 91 · see citing works
Previous maternal experience affects accumbal dopaminergic responses to pup-stimuli
Afonso, V. M., Grella, S. L., Chatterjee, D., & Fleming, A. S. (2008) · Brain Research · doi:10.1016/j.brainres.2007.12.042 · Cited by 89 · see citing works
Self-citationLonstein, J. S., & Stern, J. M. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1416 · Cited by 88 · see citing works
Self-citationKirkpatrick, B. W., Carter, C. S., Newman, S. W., & Insel, T. R. (1994) · Behavioral Neuroscience · doi:10.1037//0735-7044.108.3.501 · Cited by 86 · see citing works
Motivational aspects of maternal anxiolysis in lactating rats
Pereira, M., Uriarte, N., Agrati, D., Zuluaga, M. J., & Ferreira, A. (2005) · Psychopharmacology · doi:10.1007/s00213-005-2157-y · Cited by 80 · see citing works
“, enhancing the sensitivity of perioral and ventral-trunk regions) (Morgan et al. 1992; Stern 1990, 1996; Stern and Johnson 1990).”
BackgroundFeatherstone, R. E., Fleming, A. S., & Ivy, G. O. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.1.158 · Cited by 74 · see citing works
Self-citationNuman, M. (2020) · doi:10.1093/oso/9780190848675.001.0001 · Cited by 101 · see citing works
MAYES, L. C. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1376.018 · Cited by 79 · see citing works
Numan, M. J., FLEMING, A., & Lévy, F. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50040-3 · Cited by 63 · see citing works
Self-citationFleming, A. S., Gavarth, K., & Sarker, J. (1992) · Behavioral and Neural Biology · doi:10.1016/0163-1047(92)90122-k · Cited by 59 · see citing works
Self-citationCesarean Section or Natural Childbirth? Cesarean Birth May Damage Your Health
Chen, H., & Tan, D. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.00351 · Cited by 57 · see citing works
“Animal experiments have shown that the posterior pituitary hormone is an important intermediary in maternal behavior (Kendrick et al., 1992; Morgan et al., 1992; Porter et al., 2002; Poindron, 2005).”
BackgroundExperiential Factors in Postpartum Regulation of Maternal Care
Fleming, A. S., Morgan, H. D., & Walsh, C. J. (1996) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60336-8 · Cited by 51 · see citing works
Self-citationEarly recognition of newborn goat kids by their mother: I. Nonolfactory discrimination
Poindron, P., Gilling, G., Hernández, H., Serafín, N., & Terrazas, A. (2003) · Developmental Psychobiology · doi:10.1002/dev.10123 · Cited by 50 · see citing works
Learning during motherhood: A resistance to stress
Leuner, B., & Shors, T. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.01.002 · Cited by 49 · see citing works
“For example, oral stimulation from pup licking and ventral somatosensory stimulation from pup nuzzling, both of which are necessary for maternal responsiveness and various other aspects of maternal care, could be involved (Numan and Insel, 2003; Morgan et al., 1992; Stern, 1997).”
BackgroundRat pups are reinforcing to the maternal rat: Role of sensory cues
Magnusson, J. E., & Fleming, A. S. (1995) · Psychobiology · doi:10.3758/bf03327061 · Cited by 49 · see citing works
Self-citationThe importance of mother–infant communication for social bond formation in mammals
Okabe, S., Nagasawa, M., Mogi, K., & Kikusui, T. (2012) · Animal Science Journal · doi:10.1111/j.1740-0929.2012.01014.x · Cited by 48 · see citing works
Lonstein, J. S., Pereira, M., Morrell, J. I., & Marler, C. A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00051-x · Cited by 46 · see citing works
Noradrenergic involvement in the consolidation of maternal experience in postpartum rats
Moffat, S. D., Suh, E. J., & Fleming, A. S. (1993) · Physiology & Behavior · doi:10.1016/0031-9384(93)90192-i · Cited by 43 · see citing works
“After introduction of the pups, females were observed for 8 rain using a one-zero 5-s interval sampling procedure during which the behavior of the female was recorded every 5 s. The behaviors observed included pup sniffing, approach to pups, pup licking (general and anogenital), retrieval to nest site, and hover over…”
BackgroundMethodInfluentialSelf-citationNursing stimulation is more than tactile sensation: It is a multisensory experience
Febo, M., Stolberg, T. L., Numan, M., Bridges, R. S., Kulkarni, P., & Ferris, C. F. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.02.024 · Cited by 42 · see citing works
Olfactory-based social learning varies as a function of parity in female rats
Fleming, A. S., Kuchera, C., Lee, A., & Winocur, G. (1994) · Psychobiology · doi:10.3758/bf03327078 · Cited by 38 · see citing works
Self-citationAntenatal origins of individual differences in heart rate
DiPietro, J. A., Costigan, K. A., Pressman, E. K., & Doussard-Roosevelt, J. A. (2000) · Developmental Psychobiology · doi:10.1002/1098-2302(2000)37:4 · Cited by 71 · see citing works
Self-citationBridges, R. S., & Scanlan, V. F. (2004) · Developmental Psychobiology · doi:10.1002/dev.20038 · Cited by 32 · see citing works
Shoji, H., & Miyakawa, T. (2019) · Molecular Brain · doi:10.1186/s13041-019-0490-z · Cited by 30 · see citing works
Bornstein, M. H. (2013) · Psychology Press eBooks · doi:10.4324/9781410612144 · Cited by 27 · see citing works
Lau, B. Y. B., Layo-Carris, D. E., Emery, B. A., Everett, M., Kumar, A., Stevenson, P. K., Reynolds, K. G., Cherosky, A., Bowyer, S.-A. H., Roth, S., et al. (2020) · eNeuro · doi:10.1523/eneuro.0500-19.2020 · Cited by 24 · see citing works
Psychological and neurobiological mechanisms underlying the decline of maternal behavior
Li, M. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.06.009 · Cited by 23 · see citing works
“This is in sharp contrast to ample studies on the roles of stimulus characteristics of the young in the initiation and maintenance of rat maternal behavior, and there has been well conducted analysis of specific stimulus characteristics involved (Morgan et al., 1992; Stern, 1989, 1990; Stern et al., 1992; Stern and Ko…”
ResultBienboire‐Frosini, C., Marcet‐Rius, M., Orihuela, A., Domínguez-Oliva, A., Mora‐Medina, P., Olmos-Hernández, A. S., Casas-Alvarado, A., & Mota‐Rojas, D. (2023) · Animals · doi:10.3390/ani13030532 · Cited by 23 · see citing works
How Mothers Are Born: A Psychobiological Analysis of Mothering
Mileva‐Seitz, V. R., & Fleming, A. S. (2010) · National symposium on family issues · doi:10.1007/978-1-4419-7361-0_1 · Cited by 20 · see citing works
Self-citationPeripartum effects of synthetic oxytocin: The good, the bad, and the unknown
Rashidi, M., Maier, E., Dekel, S., Sütterlin, M., Wolf, R. C., Ditzen, B., Grinevich, V., & Herpertz, S. C. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104859 · Cited by 18 · see citing works
Carretero, M. I., Segovia, S., Espinosa-Gómez, F. C., & del Cerro, M. C. R. (2003) · Scandinavian Journal of Psychology · doi:10.1111/1467-9450.00345 · Cited by 14 · see citing works
Dye, C. N., Franceschelli, D. V., Leuner, B., & Lenz, K. M. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01624-1 · Cited by 12 · see citing works
“Somatosensory and chemosensory input from pups modulate maternal responsiveness [7, 38].”
BackgroundNaguib, M., Kober, M., & Trillmich, F. (2009) · Behavioural Processes · doi:10.1016/j.beproc.2009.10.005 · Cited by 12 · see citing works
Social play with an unfamiliar group in weanling rats (Rattus norvegicus)
Kahana, A., Rozin, A., & Weller, A. (1997) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199703)30:2 · Cited by 9 · see citing works
Self-citationMammalian NREM and REM sleep: Why, when and how
Rial, R. V., Akaârir, M., Cañellas, F., Barceló, P., Díaz, J. Á. R., Martin-Reina, A., Gamundı́, A., & Nicolau, M. C. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105041 · Cited by 11 · see citing works
“4 twitching or sucking pups, elicits immobility in the mother (Stern and Johnson, 1990; Stern et al., 1992; Pedersen, 1997; Morgan et al., 1992; Lonstein et al., 1998).”
The mother–child interface: A neurobiological metamorphosis
Cainelli, E., Vedovelli, L., & Bisiacchi, P. S. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.10.027 · Cited by 11 · see citing works
“As confirmation, vaginal delivery provides critical sensory stimulation that increases oxytocin release and helps establish maternal behaviors (Morgan et al., 1992).”
BackgroundAgrati, D., Ferreño, M., Marín, G., Uriarte, N., Zuluaga, M. J., Fernández‐Guasti, A., & Ferreira, A. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.11.002 · Cited by 10 · see citing works
Salcedo, C., Torrero, C., Regalado, M., Rubio, L., & Salas, M. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.12.020 · Cited by 9 · see citing works
Mykins, M., Layo-Carris, D. E., Dunn, L. R., Skinner, D. W., McBryar, A. H., Perez, S., Shultz, T. R., Willems, A. R., Lau, B. Y. B., Hong, T., et al. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25190 · Cited by 8 · see citing works
Stevenson, P. K., Casenhiser, D. M., Lau, B. Y. B., & Krishnan, K. (2021) · European Journal of Neuroscience · doi:10.1111/ejn.15327 · Cited by 6 · see citing works
Mykins, M., Bridges, B., Jo, A., & Krishnan, K. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1078-23.2023 · Cited by 5 · see citing works
Stress-Sensitive Parental Brain Systems Regulate Emotion Response and Motivate Sensitive Child Care
Swain, J. E. (2017) · Springer eBooks · doi:10.1007/978-3-319-65077-7_14 · Cited by 5 · see citing works
Enhanced maternal behaviors in a mouse model of congenital blindness
Bouguiyoud, N., Xie, W. B., Bronchti, G., Frasnelli, J., & Aïn, S. A. (2023) · Developmental Psychobiology · doi:10.1002/dev.22406 · Cited by 4 · see citing works
Father of mothering: Jay S. Rosenblatt
Fleming, A. S., Numan, M., & Bridges, R. S. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.01.001 · Cited by 3 · see citing works
Self-citationWalsh, C. J., Ralph, T., & Storey, A. E. (2009) · Journal of comparative psychology · doi:10.1037/a0014256 · Cited by 3 · see citing works
The biological perspective on mother-infant bonding: the importance of oxytocin
Nagasawa, M., Okabe, S., Mogi, K., & Kikusui, T. (2013) · Japanese Journal of Animal Psychology · doi:10.2502/janip.63.1.4 · Cited by 3 · see citing works
Maternal alterations induced by exposure to an unfamiliar home cage in early underfed dams
Salas, M., Regalado, M., Torrero, C., & Rubio, L. (2017) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2017.07.005 · Cited by 3 · see citing works
“…elicit deficient or inadequate maternal behavioral components and disrupt hormonal and brain changes required for the dam to adapt to the challenge of an unfamiliar cage (UC) (Smart, 1976; Morgan et al., 1992; Torrero et al., 2000; Tonkiss et al., 2003; Wu et al., 2004; LopezJimenez et al., 2013).”
BackgroundEffects of Prenatal Cocaine on Maternal Care and Ultrasonic Vocalizations of Rat Offspring
McMurray, M. S., & Johns, J. M. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-809600-0.00043-3 · Cited by 3 · see citing works
Salas, M., Ortiz‐Valladares, M., Regalado, M., & Torrero, C. (2020) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2020.1012034 · Cited by 3 · see citing works
A Rodent Model of Cocaine’s Effect on the Mother Infant Dyad
McMurray, M. S. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/ddyd-r062 · Cited by 3 · see citing works
Li, M. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1394201 · Cited by 2 · see citing works
Neuroendocrine Regulation of Maternal Behavior
Bridges, R. S., & Byrnes, E. M. (2000) · Humana Press eBooks · doi:10.1007/978-1-59259-707-9_17 · Cited by 2 · see citing works
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0008 · Cited by 2 · see citing works
Hormonal Control of Maternal Behavior in Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0003 · Cited by 2 · see citing works
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0002 · Cited by 1 · see citing works
Imaging the Maternal Rat Brain
Febo, M., & Ferris, C. F. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-374285-8.00004-4 · Cited by 1 · see citing works
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0001 · Cited by 1 · see citing works
Central Neural Circuits Regulating Maternal Behavior in Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0005 · Cited by 1 · see citing works
Alloparental Behavior and Paternal Behavior in Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0007 · Cited by 1 · see citing works
Cox, E. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/d30h-ym54
Evolutionary Perspectives on the Parental Brain
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0011
Anxiety Reduction and Maternal Aggression in Postpartum Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0006
Development of the Parental Brain in Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0009
Development of the Parental Brain in Humans
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0010
Brain Mechanisms Regulating Maternal Behavior in Nonhuman Mammals
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.003.0004
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.002.0006
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.002.0003
Abbreviations Used for Major Brain Regions
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.002.0007
Numan, M. (2020) · Oxford University Press eBooks · doi:10.1093/oso/9780190848675.002.0004
Salas, M., Torrero, C., & Regalado, M. (2025) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2025.155006
- Authors
- Morgan, H. D., Fleming, A. S., & Stern, J. M.
- Affiliations
- University of Toronto (CA)
- Rutgers, The State University of New Jersey (US)
- Corresponding author
- Fleming, Alison S.
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 1992-03
- Volume
- 51
- Issue
- 3
- Pages
- 549-555
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W2068523411
- Cited by
- 93
- References
- 36
- Citations by year
- 2025: 1 · 2024: 3 · 2023: 5 · 2022: 1 · 2021: 1 · 2020: 19 · 2019: 4 · 2018: 1 · 2017: 3 · 2016: 1 · 2015: 2 · 2014: 2 · 2013: 2 · 2012: 2
- FWCI
- 6.87
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- maternal behavior, maternal responsiveness, lidocaine, mystacial pad, primiparous rats, maternal experience
- MeSH terms
- Animals, Female, Maternal Behavior, Mechanoreceptors, Rats, Inbred Strains, Reaction Time, Retention, Psychology, Sensation, Sensory Deprivation, Skin, Touch, Vibrissae, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
