Differential emotional experience induces elevated spine densities on basal dendrites of pyramidal neurons in the anterior cingulate cortex of Octodon degus

It appears likely that, in analogy to the synaptic development of sensory and motor cortices, which critically depends on sensory or motor stimulation (Rosenzweig and Bennett, 1996), the synaptic development of limbic cortical regions are modulated by early postnatal cognitive and emotional experiences. The very first postnatal experience, which takes place in a confined and stable familial environment, is the interaction of the newborn individual with the parents and siblings (Gray, 1958). The aim of this quantitative morphological study was to analyze the impact of different degrees of juvenile emotional experience on the synaptic development in a limbic cortical area, the dorsal anterior cingulate cortex, a region which is involved in the perception and regulation of emotions. We study the precocious trumpet-tailed rat (Octodon degus) as the animal model, because, like human babies, this species is born with functional visual and acoustic systems and the pups are therefore capable of detecting even subtle environmental changes immediately after birth (Reynolds and Wright, 1979; Poeggel and Braun, 1996; Braun et al., 2000; Ovtscharoff and Braun, 2001). The results demonstrate that already a subtle disturbance of the familial environment such as handling induced significantly elevated spine densities on the basal dendrites of layer III cortical pyramidal neurons. More severe disturbances of the emotional environment, such as periodic parental deprivation with or without subsequent chronic social isolation, resulted in an elevation of spine densities of similar magnitude as seen after handling and in addition, altered spine densities confined to specific dendritic segments were observed in these groups. These observations unveil the remarkable sensitivity of the dorsal anterior cingulate cortex towards environmental influences and behavioral experiences during phases of postnatal development. The behavioral consequences of these experience-induced synaptic changes still need to be analyzed further to assess if they are beneficial or detrimental to the animals cognitive and emotional capacities in later life.

[1]  K. Braun,et al.  Quantitative changes in reduced nicotinamide adenine dinucleotide phosphate-diaphorase-reactive neurons in the brain of Octodon degus after periodic maternal separation and early social isolation , 2000, Neuroscience.

[2]  V. Denenberg,et al.  Commentary: is maternal stimulation the mediator of the handling effect in infancy? , 1999, Developmental psychobiology.

[3]  K. Braun,et al.  Recognition of Mother's voice evokes metabolic activation in the medial prefrontal cortex and lateral thalamus of Octodon degus pups , 2001, Neuroscience.

[4]  K. Braun,et al.  Blockade of N-methyl-D-aspartate receptor activation suppresses learning-induced synaptic elimination. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[5]  P. Gray Theory and Evidence of Imprinting in Human Infants , 1958 .

[6]  S. Korchin,et al.  The effects of early shock and handling on later avoidance learning. , 1956, Journal of personality.

[7]  J. Wright,et al.  Early postnatal physical and behavioural development of degus (Octodon degus) , 1979, Laboratory animals.

[8]  D. Winfield The postnatal development of synapses in the different laminae of the visual cortex in the normal kitten and in kittens with eyelid suture. , 1983, Brain research.

[9]  M. Metzger,et al.  Maternal separation and early social deprivation in octodon degus: quantitative changes of nicotinamide adenine dinucleotide phosphate-diaphorase-reactive neurons in the prefrontal cortex and nucleus accumbens , 1999, Neuroscience.

[10]  K. Braun,et al.  Maternal separation and social isolation modulate the postnatal development of synaptic composition in the infralimbic cortex of Octodon degus , 2001, Neuroscience.

[11]  K. Braun,et al.  Juvenile emotional experience alters synaptic inputs on pyramidal neurons in the anterior cingulate cortex. , 2001, Cerebral cortex.

[12]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  L. Descarries,et al.  Increased number and size of dendritic spines in ipsilateral barrel field cortex following unilateral whisker trimming in postnatal rat , 1998, The Journal of comparative neurology.

[14]  C. Horner,et al.  Methods of estimation of spine density--are spines evenly distributed throughout the dendritic field? , 1991, Journal of anatomy.

[15]  P. Huttenlocher Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[16]  M. Kossut Experience-dependent changes in function and anatomy of adult barrel cortex , 1998, Experimental Brain Research.

[17]  K. Braun,et al.  Early auditory filial learning in degus (Octodon degus): behavioral and autoradiographic studies , 1996, Brain Research.

[18]  M. Metzger,et al.  Maternal separation followed by early social deprivation affects the development of monoaminergic fiber systems in the medial prefrontal cortex of Octodon degus , 1999, Neuroscience.

[19]  A. Riesen,et al.  Deprived somatosensory‐motor experience in stumptailed monkey neocortex: Dendritic spine density and dendritic branching of layer IIIB pyramidal cells , 1989, The Journal of comparative neurology.

[20]  C. Horner,et al.  Neural plasticity of the hippocampal (CA1) pyramidal cell--quantitative changes in spine density following handling and injection for drug testing. , 1991, Journal of anatomy.

[21]  O. Périer,et al.  Deprivation and morphological changes in the central nervous system. , 1986, Acta oto-laryngologica. Supplementum.

[22]  R. Sapolsky,et al.  Postnatal handling attenuates certain neuroendocrine, anatomical, and cognitive dysfunctions associated with aging in female rats , 1991, Neurobiology of Aging.

[23]  P. Rakić,et al.  Tempo of neurogenesis and synaptogenesis in the primate cingulate mesocortex: Comparison with the neocortex , 1995, The Journal of comparative neurology.

[24]  E. Bennett,et al.  Psychobiology of plasticity: effects of training and experience on brain and behavior , 1996, Behavioural Brain Research.