Environmental Influences on Neural Plasticity, The Limbic System, Emotional Development and Attachment (Reprinted from: Child Psychiatry and Human Development,29, 187-203, 1999)
by Rhawn Joseph, Ph.D.
Rhawn Gabriel Joseph, Ph.D.
The effects of early environmental influences on neural plasticity, the limbic system, and social and emotional development are examined, an illustrative case the "Unabomber" is presented. Deprived or abnormal rearing conditions induce severe disturbance in all aspects of social and emotional functioning, and effect the growth and survival of dendrites, axons, synapses, interneurons, neurons, and glia. The amygdala, cingulate, and septal nuclei develop at different rates which correlate with the emergence of wariness, fear, selective attachments, play behavior, and the oral and phallic stages of development. These immature limbic nuclei are "experience-expectant," and may be differentially injured depending on the age at which they suffer deprivation. The medial amygdala and later the cingulate and septal nuclei are the most vulnerable during the first three years of life. If denied sufficient stimulation these nuclei may atrophy, develop seizure-like activity or maintain or form abnormal synaptic interconnections, resulting in social withdrawal, pathological shyness, explosive and inappropriate emotionality, and an inability to form normal emotional attachments.
NEURAL PLASTICITY, THE LIMBIC SYSTEM, EMOTIONAL DEVELOPMENT & ATTACHMENT
The human brainstem is almost fully functional at birth whereas the limbic forebrain is more plastic, "experience-expectant," and slower to mature and develop. 1-13 Whereas the brainstem mediates reflexive motor and vital functions, 9 the limbic forebrain (e.g. the hypothalamus, amygdala, septal nucleus, cingulate, and hippocampus) monitors and attempts to satisfy hunger and thirst and is responsible for the experience and expression of emotions including pleasure, rage, fear and joy and the desire for social-emotional contact. 6-8
Unlike the brainstem which is more "hard wired" and initially under direct genetic and reflexive sensory control, 9 limbic system nuclei, such as the amygdala, septal nuclei and hippocampus, as well as the later to mature neocortex, require considerable social, emotional, perceptual, and cognitive stimulation during the first several months and years of life in order to develop normally. If sufficient stimulation is not provided, or if exposed to an abnormal or neglectful environment, developing neurons and dendrites will establish or maintain aberrant, abnormal interconnections, or whither, die, and drop out at an accelerated rate. 6-8,10-25
Initially billions of neurons, dendrites and synaptic interconnections are produced in random excess. 4-6 Over the first several years and decade of life, these excess neurons are pruned and sheared away by the hundreds of millions. Although additional neurons continue to be generated even in the adult brain, it is through dendritic attrition that specific neural networks are sculpted and formed. The sculpting of specific neural pathways fine tunes perception, selective attention, and promotes learning, memory, and cognitive and personality development.
However, if reared in an abnormal, deprived and socially isolated environment, limbic system nuclei will atrophy, random interconnections will be maintained, or neural pathways will develop abnormally. 6-8,10-19,36 Neurons, dendrites and interconnections that would normally survive are significantly reduced throughout the brain. There is an accelerated loss of presynaptic vesicles, glia, interneurons, neurons, axons, synapses, and cortical thickness, and the septal nuclei, amygdala and hippocampus may develop seizure-like activity. 6-8,10-25 An abnormal or impoverished rearing environment can decrease a thousand fold the number of synapses per axon, and retard the growth and eliminate billions if not trillions of synapses per brain 20 and result in the preservation of abnormal interconnections which are normally discarded over the course of development.
Because the brain's developmental journey does not cease at birth 1-7 early environmental influences can determine the establishment of specific neural networks, or can lead to the creation and maintenance of aberrant or random neural pathways thus interfering with the forebrain's ability to discretely, purposefully, and selectively maintain control over behavior. 6-8,21-29 Hence, in summary, early social, emotional and environmental influences exert significant organizing effects not only on the brain but shape and mold all aspects of intellectual, perceptual, and social and emotional development. 6-8, 26-45
DEPRIVATION, NEURAL COMPETITION & PERCEPTUAL BLINDNESS
Abnormal and deprived experience during early critical developmental periods may even induce perceptual blindness secondary to functional invasion and occupation by competing neuronal cell assemblies which take over those neurons that have been insufficiently or adversely stimulated. 6,21-25,46 For example, in non-human primates, if one eye is sutured shut soon after birth and patterned visual input is prevented from reaching target cells in the lateral geniculate nucleus of the thalamus and visual neocortex, target neurons and cellular layers and columns become smaller and functionally suppressed by adjacent cells receiving normal input. 21-26 Cortical columns and layers innervated by the deprived eye shrink and those of the experienced eye grow larger, filling in the vacated space. 21,22,24 Perceptual functioning becomes exceedingly abnormal and the deprived eye is unable to see objects, places, or smiling faces.
Moreover, in monkeys, with visual deprivation, the superior parietal lobe suffers a 92% reduction in visually responsive neurons in multi-modal area 7, whereas the number of parietal neurons responsive to tactile somesthetic stimulation increases by up to 117%. 25 Similarly, in mice, the auditory cortex also exponentially increases by default, taking over abandoned cortical territory left behind by the retreating population of formerly visually responsive neurons whose cortical territory substantially shrinks in size. 23 Hence, early visual deprivation limited to one eye results in a massive abandonment of "visual" neurons throughout the brain and leads to their acquisition by cells receiving different forms of input.
In primates, if lid sutures are reversed and the visually deprived eye is opened, the subject appears to be blind, although the eye is normal. 26-27 The deprived eye has become functionally disconnected from the thalamus and visual cortex.
Blindness following monocular visual deprivation is due to insufficient visual stimulation during this early critical period of development, and is directly attributable to the competitive influences of normal neurons which invade, conquer and take over vacant (or inactive) cortical space. These invading and retreating neurons prevent the transfer and neocortical reception of visual input transmitted from the inexperienced eye which is now functionally blind.
Be it animal or human, similar deprivation-induced abnormalities affect the limbic system which may become emotionally and socially "blind" and unable to perceive, process, or respond in a normal fashion to social and emotional stimulation. 6-8,29 Because various limbic neural assemblies require considerable social and emotional experience during specific developmental periods, and are thus "experience-expectant," they fail to fully develop or no longer function normally if deprived of that experience, even when "normal" experience is later provided.
Indeed, humans and animals reared in an abnormal, or deprived and socially and maternally impoverished environment typically display significant reductions in learning, perceptual, intellectual and memory capacity, as well as diminished curiosity and exploratory behavior. 6-8,14-15,26-37 These environmentally induced deficits include a reduced ability to anticipate consequences or to inhibit irrelevant or inappropriate, self-destructive behaviors, and humans and other animals demonstrate severe disturbances in all aspects of social emotional expressive and perceptual functioning.
ABNORMAL EARLY SOCIAL & EMOTIONAL LIMBIC SYSTEM DEVELOPMENT
As with the visual system, similar "experience-expectancies" characterize social and emotional development and the formation of loving attachments. 6-8,29-31,33-35,40-43, 47-50 The infant (and its limbic system) requires considerable social and physical stimulation, including emotionally "sensitive" maternal contact. So pervasive is this limbic need for emotional stimulation that during much of the first year of life children will indiscriminately seek social contact and will smile at the approach of anyone, even complete strangers. 7,51-52 Indiscriminate contact seeking and attachment during early development maximizes opportunities for physical-social interaction and provides the experience-expectant stimulation that the infant's developing limbic system requires in order to develop and function in a normal manner. 6-8
So intense is the "experience-expectant" and limbic need for physical and social contact that young animals raised in social isolation will form attachments to bare wire frames, inanimate objects, television sets, as well as to animals that might maul them and creatures that might eat them. 7,33,54-56 Infant humans will desperately seek contact even with mothers who violently reject and physically abuse them. 6-7 So pervasive is this need for social stimulation that when grossly reduced or denied, the result may be death.
For example, in several well known studies of children raised in foundling homes during the early 1900's, when the need for emotional contact was not well recognized, morbidity rates for children less than 1 year of age was generally over 70%. Of 10,272 children admitted to the Dublin Foundling home during a single 25 year period, only 45 survived. 6-7 Children who survive an infancy spent in institutions where mothering and contact comfort were minimized, display low intelligence, extreme passivity, apathy, severe attentional deficits, pathological shyness, and exceedingly bizarre social behavior. 6-7,30-35,40-43
R.A. Spitz, 34,35 studied over 100 children reared in a foundling home where mothering and social stimulation was minimal. Spitz found that within one year these children became unresponsive to social stimulation, and would lay passively on their beds. These unmothered children made vigorous attempts to avoid strangers or novel objects or toys, and when approached they would scream and withdraw. These deprived youngsters spent hours engaged in obsessive, repetitive, stereotyped and bizarre self-stimulating movements; i.e. rocking, head banging, or pinching precisely the same piece of skin until sores developed. Most of these children became permanently emotionally and socially disabled.
These abnormalities are not limited to humans but affect other primates and mammals including dogs. 33,53-56 For example, as detailed by Harlow (p. 138), 33 infant monkeys raised alone with surrogate terry cloth mothers would stereotypically "sit in their cages and stare fixedly into space, circle their cages in a repetitive stereotyped manner and clasp their heads in their hands or arms and rock for long periods of time. They developed compulsive habits, such as pinching precisely the same patch of skin on their chest between the same fingers hundreds of times a day; occasionally such behavior may become punitive and the animal may chew and tear at its body until it bleeds."
LIMBIC SYSTEM SOCIAL-EMOTIONAL DEVELOPMENT
As is now well established, the limbic system provides the foundation for all aspects of social and emotional behavior. 6-8,29,36,57-68 However, limbic system nuclei, such as the amygdala, septal nuclei, and cingulate gyrus, play different roles in social and emotional development. 6-8,57-68 They also mature at different time periods. 1-2,6-8
As first discovered and detailed by Joseph, 6-8 different phases of social emotional development and the formation of loving attachments correspond to the differential maturation rates of the amygdala, septal nuclei, and cingulate gyrus; a developmental process that also involves the orbital frontal lobes. 69,70 The orbital frontal lobes are an evolutionary derivative of the amygdala and cingulate, and remain quite plastic for the first several years and even decades of life. 6-9
The differential maturational rates of these limbic nuclei, beginning with the development of the amygdala and followed by the cingulate and septal nuclei, enables humans and other higher mammals to first socialize indiscriminately, to slowly develop stable and selective loving attachments, and, around six months to one year of age, to express and experience emotions such as anger, joy, and fear of strangers. 30,47,52,69-73
For example, the medial amygdala rapidly develops and completes its myelogenetic cycle of maturational development by the end of the first postnatal year. 2 It is the immature amygdala which is responsible for the extreme orality and indiscriminate socializing of the infant; interaction which it requires in order to mature normally. 6-8 As fear and wariness are hallmarks of amygdala activity, 6-8, 57,58,62 it is the continued maturation of this nucleus which is also responsible for the experience of wariness and then a fear of strangers. 6-8
Although somewhat slower to develop, the cingulate gyrus also reaches an advanced stage of maturity during the first year, but continues to develop over the course of the next several years. 2 The cingulate gyrus, being intimately associated with the amygdala and orbital frontal lobes, also contributes to the establishment of infant-maternal attachment during the latter half of the first postnatal year, including the expression of maternal separation anxiety. 7,62 The cingulate is capable of considerable emotional flexibility, engages in role playing, and can mimic and express emotional states which it does not feel. 7,62-64 Hence, as the cingulate gyrus (and frontal lobes) continues to mature, additional cingulate activities emerge, 7 such as complex play activities, role playing, and creative fantasy which emerges around age three. 47,70
By contrast, the septal nuclei undergoes a more protracted rate of development and does not begin to reach adult levels until three years of age; 2,7 a process of development which actually continues well into puberty. 6-8 However, between the ages of one and three, as it begins to mature, the septal nuclei inhibits and counters the indiscriminate social desires of the amygdala and contributes to a narrowing of social contact seeking and the generation of wariness of strangers. 6-8 In addition, whereas the immature amygdala is associated with the oral stage, the development of the so called phallic stage of psychosexual development could be viewed as representing an advanced stage of septal maturation, 7 as septal stimulation induces penile erection and clitoral engorgement. 6-8,62
AMYGDALA & SEPTAL SOCIAL-EMOTIONAL ATTACHMENT & DEVELOPMENT
It is well established that the amygdala mediates most aspects of social and emotional behavior including emotional memory, attention, arousal, and the experience of love, fear and joy. 6-8,29,36,57-62 The amygdala promotes the desire for social and emotional stimulation and loving physical interaction, responds vigorously to physical caresses, and contains facial recognition neurons which discern the emotional significance of different facial expressions 6-8,57,58,61,62,74 It is the infant's amygdala which selectively attends to and responds to the human face and which prefers faces to other stimuli; 7 a characteristic of most infants which becomes enhanced with age. 47,51,52,71-73
Corresponding with the maturation of the contact loving amygdala, the infant becomes increasingly socially oriented, and its emotional repertoire becomes more expansive, such that the ability to experience and express a wider range of emotions gradually develops with wariness and then fear appearing around six months of age. 6-8, 47,71-73 Hence, until six to months the child will smile (or at least stare) at the approach of anyone, even complete strangers. They may also vigorously protest separation from strangers (e.g. if they leave the room); a function of the social stimulus hunger experienced by the immature and contact loving amygdala. 6-8 Hence, infants less than six months will also readily accept mother substitutes. However, as the cingulate and septal nuclei begin to mature, counterbalancing influences are brought to the fore, and infants begin to become easily upset at the prospect of maternal separation. 7,30,31,47,71-73
As the inhibiting septal nuclei, cingulate gyrus and the orbital frontal lobes mature, the desire for social contact becomes increasingly narrow, focused, inhibited, selective, and discriminating. Hence, between seven to eleven months of age, infants no longer respond in a generalized and indiscriminately friendly fashion. They increasingly bond to their mothers, show separation anxiety, and are more likely to restrict their smiling and socializing to familiar faces and specific members of their family. 7,30,31,47,71-73
Thus during the septal, cingulate, and orbital frontal developmental stage, generalized social contact seeking, which is initially mediated by the amygdala, becomes increasingly inhibited, restricted and focused on just a few individuals. Moreover, around seven to eleven months of age children begin to avoid and show fear and anxiety when strangers approach or enter the house 7,30,31,47,71-73 By 9 months, 70% of children may respond aversively if a stranger approaches, whereas by 10 months they might cry out. By one year up to 90% of children may respond aversively to strangers; a function of the combined influences of the amygdala, cingulate gyrus, and still immature septal nucleus. 6-8
Thus in summary, during the amygdaloid maturational phase there is indiscriminate orality and social contact seeking. The contact-loving amygdala expresses its experience-expectant needs unhindered as the septal nucleus, cingulate and orbital frontal lobes have not yet sufficiently matured so as to inhibit and counterbalance these tendencies. As these nuclei mature and counterbalancing influences are brought to the fore, the indiscriminate orality and contact seeking of the amygdala begins to wane, and the infant begins to express separation anxiety and fear of strangers. As the cingulate and septal (and amygdala) nuclei continue to mature, orality is replaced by the so called phallic stage, and the infant engages in creative fantasy and role playing. Again, however, these nuclei have different roles in social emotional functioning, and in some respects complement as well as counterbalance and inhibit one another.
Hence, if the septal nuclei were subsequently destroyed, the amygdala would again respond in a socially indiscriminate fashion. 6-8 However, if the orbital frontal lobe or cingulate were destroyed, separation anxiety and flights of fantasy disappear and the amygdala is disconnected from the neocortex. In consequence, emotional behavior and contact seeking would be blunted. In fact amygdala, orbital or cingulate destruction induces a severe social and emotional agnosia, and victims generally avoid all social contact and lose the ability to react in an appropriate emotional fashion. 6-8,59,60,62-68 Indeed these findings may well explain why emotionally blunted, socially withdrawn, early onset schizophrenics not uncommonly have abnormalities and lesions localized to the septal nuclei, or amygdala, hippocampus, or temporal (or frontal) lobe. 6,8,18,29,58,75-79
Unfortunately, if reared in an abnormal, deprived, neglectful, or abusive environment, the amygdala, septal nuclei, cingulate gyrus, and the hippocampus may develop abnormally, and suffer environmentally induced lesions. Because the developing limbic system is experience-expectant, children and animals deprived of these expected experience behave in a fashion which is identical to those who have suffered limbic system destruction or amputation.
AMYGDALA & SEPTAL DESTRUCTION & SOCIAL-EMOTIONAL ABNORMALITIES
If reared under neglectful, stressful, or abusive conditions the amygdala, septal nuclei, and the hippocampus may atrophy or develop seizure-like activity, referred to as kindling. 8,10,11,13-19,29,36,87,88 Abnormal seizure-like activity, however, often has a hyperactivating influence, such that tendencies normally associated with the afflicted part of the brain may be exaggerated. For example, heightened and abnormal septal activity may increase and exaggerate the inhibitory influences this structures exerts on various portions of the amygdala, hypothalamus, and hippocampus. By contrast, septal atrophy or destruction not only results in functional loss but a disconnection syndrome. 6-8,29 In consequence, tissues such as the amygdala or hippocampus are no longer subject to septal counterbalancing influences and will therefore function abnormally.
For example, whereas seizure activity or abnormal septal hyperactivity may induce extreme social withdrawal and indifference, septal destruction triggers an extreme desire for social and physical contact coupled with aggressive, assaultive and bizarre behavior. 80-82 This social-bullying behavior is in part due to the abnormal effects on and release of the amygdala from the septal's counterbalancing influences. 6-8 The contact-loving amygdala ceases to be restrained and also functions abnormally.
With bilateral septal nuclei destruction the drive for social contact becomes irresistible. Septally lesioned animals will even seek out species which they normally avoid, fear or dislike; 80-82 a consequence of amygdala disinhibition. Rats with septal lesions will seek mice and rabbits (which they usually avoid) and will hug and cuddle nasty tempered cats. If a group of septally lesioned animals are placed together, extreme huddling results; a consequence, again, of the removal of septal counterbalancing influences on the contact loving amygdala.
If other animals are unavailable they will seek out, cling to and hug blocks of wood, old rags, or bare wire frames. Indeed, these behaviors are identical to that of animals and humans reared under isolation. 33-35,41-43,53-56 However, although seemingly starved for social stimulation, septally lesioned animals also become explosively violent; 6-8,62,80-82 This behavior is similar to that of humans who suffered maternal deprivation late in development. 33-35,41-43
However, if the amygdala is destroyed, emotional functioning is virtually extinguished and the desire for social contact is essentially abolished. 59,60,65-68,83 Among humans, non-human primates, and mammals, bilateral destruction of the amygdala significantly disturbs the ability to behave in a socially normal manner, or to determine, discern, or identify motivational and social-emotional nuances, including facial expressions or body language. 6-8,59,60,65-68,83
Animals or humans with bilateral amygdaloid destruction respond in an emotionally blunted fashion, and become pathologically shy and "blind" and "deaf" to the social, emotional or motivational characteristics of their environment. This social-emotional agnosia includes even the ability to feel love or affection. 65-68 Amygdalectomized humans cease to respond in an appropriate emotional manner to friends, staff or family, and behave as if they no longer recognized those who they formerly dearly loved. Instead they engage in extreme orality, may masturbate frequently (septal release) and avoid all contact with others, preferring to sit alone in isolation. 65-68
Among primates who have undergone bilateral amygdaloid removal, once released from captivity and allowed to return to their social group, a social-emotional agnosia becomes readily apparent. 59,60 They become emotionally blind and no long respond to and seem unable to appreciate or understand emotional or social nuances. 59,60,83 Like amydalectomized humans, 65-68 these animals lose all interest in social activity and persistently attempt to avoid contact with others. If approached they withdraw. If followed they flee.
Even maternal behavior is severely affected. According to Kling, 59 mothers will bite off fingers or toes, break arms or legs, and behave as if their "infant were a strange object to be mouthed, bitten and tossed around as though it were a rubber ball".
DEVELOPMENTAL & SURGICALLY INDUCED LIMBIC LESIONS: PARALLEL SYMPTOMS
The maternal behavior of primate mothers with bilateral amygdala destruction is identical to the maternal behavior of primate mothers who were raised in isolation and without mothering. For example, compare Kling's description (above) with that of Harlow 33 (pp. 256-257, 259): "After the birth of her baby, the first of these unmothered mothers ignored the infant and sat relatively motionless at one side of the cage, staring fixedly into space hour after hour. As the infant matured desperate attempts to effect maternal contact were consistently repulsed... Other motherless monkeys were indifferent to their babies or brutalized them, biting off their fingers or toes, pounding them, and nearly killing them until caretakers intervened. Despite the consistent punishment, the babies persisted in their attempts to make maternal contact."
Not only do motherless mothers behave like mothers with amygdala destruction, but infants raised in isolation behave similarly to amygdalectomized animals. Both groups demonstrate a pronounced tendency to actively seek out painful and dangerous external stimuli 53-56,83 For example, Kluver and Bucy, 83 reported that amygdalectomized primates would repeatedly touch and mouth a burning flame. Similarly, Melzack and Scott, 56 found that puppies raised for seven months in isolation would repeatedly stick their snouts into burning flames. Moreover, when Melzack and Scott stuck pieces of glass or burning matches into their snouts, these poor creatures made no attempt to escape but would hover excitedly right next to their tormentors.
Abnormal rearing conditions produce social, emotional, and maternal deficits similar to amygdala destruction because the amygdala (as well as the septal nuclei and cingulate gyrus) is adversely affected when normal "experience-expectancies" fail to be met. As these nuclei require social emotional stimulation during early development, if that stimulation is insufficient or abnormal, these limbic system nuclei will fail to function or develop normally, thus producing disturbances identical to those following their destruction.
However, these pathological consequence are not just a function of lack of appropriate experience, but a result of the stress and emotional trauma associated with neglectful conditions. Deprivation is stressful, 19,29,30,31,34,35,84,85 and the stress of neglect alters not just nerve cells, but their neurochemistry, including the secretion of neurotransmitters which are important in regulating neural development and neural plasticity. 29,84,85
NOREPINEPHRINE, DEPRIVATION & LIMBIC SYSTEM NEURAL PLASTICITY
Norepinephrine (NE) exerts a stimulating effect on neural growth, significantly influences neuronal maturation and promotes neural plasticity and synaptic development during the early stages of pre- and post-natal development. 29,84-89 Moreover, among its many activities, NE serves a neuronal protective function, and when depleted, such as in response to chronic stress neurons are exposed to the debilitating effects of enkephalins and corticosteroids 29,36,37,90-92 --stress hormones released as part of the "fight or flight" stress response. Unfortunately, NE neurotransmitters may fluctuate wildly in response to even mildly adverse early experiences including temporary separation from the mother. 29,84,85
In consequence, aberrant neural growth and atrophy may be induced, including the formation of abnormal neural networks. 29,36,37,84-89,90-92 These disruptive deprivation and stress induced effects are especially pronounced within the amygdala, septal nuclei, and the hippocampus, and can lead to abnormal seizure-like activity, such as kindling. 7,8,18,29,36,37,78,79,90-92 However, if the amygdala, septal nuclei and hippocampus are injured or abnormally activated, not just emotional functioning, but the ability to remember those who are emotionally significant is disrupted.
DEPRIVATION, MEMORY, ATTACHMENT & THE HIPPOCAMPUS
The ability to form emotional attachments requires not just emotional stimulation, but the capacity to remember faces, people, objects, and even locations; functions associated with the amygdala and hippocampus. 6-8,29,36,37,57,58,62,74,90,92-96 Humans and other animals form attachments to people, other animals, and inanimate objects, and even primitive creatures display attachments to specific locations, e.g. their home base.
However, as the amygdala and hippocampus may be injured by deprivation or abnormal rearing experiences, not just emotionality, but all aspects of short-term and long-term memory functioning may be disrupted as well; 6-8,29,36,37,57,58,62,74,90-96 including the ability to remember those who are emotionally significant. 7,8,29,36,37 If subject to repeated instances of neglect and abuse, these conditions can induce a traumatic amnesia so profound that even friends and loved ones are forgotten. 8,29,36,37
In fact, just as temporary separation from the mother can induce significant alterations in NE and damage the amygdala, brief (albeit repeated) as well as long term instances of deprivation, stress, and abuse, can produce hippocampal atrophy in humans and animals. 8,13-15,29,36,37,90,91 Hippocampal pyramidal dendrites are pruned away by the millions. 36,37,90,91 Moreover, the stress induced depletion of NE coupled with excessive secretion of corticosteroids and enkephalins can hyperactivate hippocampal pyramidal neurons and eliminate hippocampal theta and long term potentiation 36,37,90,91 --prolonged neural excitation associated with learning and memory.
Of course, if the hippocampus is injured and cannot learn and remember, it cannot assist in the formation of attachments to objects, locations, or familiar faces. Consider, for example, the famous case of H.M, who underwent the surgical removal of both hippocampi. 92 Brenda Milner has worked with H.M, for over 25 years, yet she is an utter stranger to him.
TEMPORARY SEPARATION & PROGRESSIVE DETERIORATION
The limbic system and all aspects of social and emotional functioning can be negatively impacted by emotional trauma, neglect, abuse, and in response to even temporary separation from the mother. However, these deleterious consequences also become more severe and permanent as the trauma and separation becomes increasingly prolonged. 31,34,35-37,41-43
For example, Spitz, 34,35 found that children younger than age two who were hospitalized, separated from families and isolated from their mothers would pass through up to three stages of emotional turmoil depending on the length of their stay. The first phase often developed within minutes, and was characterized by a protest period where children would frequently cry and scream for their mothers. In some cases this protest phase lasted several days or weeks. If the separation continued this was followed by a stage of despair in which the children would cease to cry, lose interest in the environment and withdraw. In the final stage the children ceased to show interest in others and no longer responded to affection. Instead they became passive and unresponsive, sitting or lying quite still with a frozen expression, staring for hours at nothing. If the separation continued there was further deterioration, with children becoming ill or dying.
Those who were returned home after just a few weeks of separation would desperately cling to their mother, follow them everywhere, and demonstrated extreme fearfulness when left alone even for short time periods. 31,34,35 Those who were deprived of maternal contact for six months or more instead behaved in a withdrawn, depressed and disinterested manner and were unable to reestablish their normal attachment to their mother. According to Bowlby, 31 children who suffer long-term or repeated separations during the first three years of life are usually permanently disabled.
These consequences are seemingly permanent due to the catastrophic effects early deprivation induces within the limbic system and related brain structures. However, depending on a number of factors including age, genetic predispositions, and the length of deprivation or inadequate mothering, as well as the quality of the mothering when she is present, different aspects of social-emotional development and different limbic system nuclei may be affected. This is because the amygdala, septal nuclei, cingulate and orbital frontal lobes mature at different rates and become more or less vulnerable at different time periods.
For example, monkeys deprived of maternal contact for the first three months after birth become severely withdrawn, self abusive, and bizarre, and scream and withdraw if touched or approached. Those deprived for six months become severely autistic, and the desire for social contact is completely abolished. 33
Similarly humans placed in foundling homes soon after birth become the most bizarre, autistic, self- abusive, and self-stimulating and are the most likely to respond with "blood curdling screams" if strangers approach. 34,35,41-43 Be it human or primate, these deficits are secondary to massive environmentally induced injury to the amygdala which is most vulnerable during this period of life.
By contrast, children placed in foundling homes after they have reached six months or even one year of age, although socially bizarre, violent and aggressive, often respond to strangers with extreme stickiness and persistently express an intense desire for social cohesion. 34,35,41-43 That is, they crave social stimulation while simultaneously behaving in a pathologically shy, bizarre, aggressive, and inappropriate fashion. Those placed in an institution after age one, although aggressive, unfriendly, shy, and socially bizarre also display an insatiable need for attention and affection. 41-43 These deficits are reminiscent of septal destruction and are likely due to an environmental injury to the septal nuclei which becomes more vulnerable from the first to third year of life.
Hence, deprivation in humans and non-human primates that begins soon after birth and which continues for six months or longer results in the most profound disturbances of social-emotional functioning, in part because the amygdala and other still maturing limbic nuclei are directly impacted. However, if some social and emotional stimulation is provided for the first several months, those limbic and amygdala neurons whose experience-expectancies were briefly met tend to survive and function somewhat normally. By contrast, if deprivation or abnormal experience is provided later in development, limbic structures such as the septal nuclei are more severely affected. Like those with septal destruction, children deprived later in life may crave social contact, but behave in a shy, bullying, and socially inappropriate manner.
SPECULATIONS ON THE BRAIN OF THE UNABOMBER
The deleterious consequences of even short-term deprivation and maternal neglect is not purely a function of the nature of the environment, as genetic and predisposing factors are also contributory. Consider, the case of Ted Kaczynski, the "Unabomber."
Ted Kaczynski lived as a hermit in small isolated cabin in Montana, and was arrested, after a rein of terror in which he constructed and employed small bombs in order to kill and maim over a dozen individuals. Ted became ill and was hospitalized and completed isolated at 8 to 9 months of age and was deprived of maternal and loving contact for 1-2 weeks. 97 During that period (as reported by his mother), he developed and demonstrated all the classic signs of "hospitalism" and rapidly passed through all three stages associated with deprivation, from protest to unresponsiveness, as described by Spitz. 34,35
Moreover, after he returned from the hospital all aspects of social and emotional functioning became bizarre, and he ceased to respond to affection or social stimulation. He became pathologically shy, severely withdrawn, unable to relate, sexually confused, even seeking a sex change operation, and was almost completely disinterested in interacting with others unless it was indirect and carried on through his extensive writings (hypergraphia). Hypergraphia, however, is a classic sign of amygdala-temporal lobe dysfunction. In all other respects he was a social recluse. If approached he would withdraw and become upset. 97 However, he also sometimes felt a craving for social stimulation that he was unable to satisfy due to his shyness and inability to relate in a normal fashion. Indeed, he not only blew people up, but would sometimes behave in a mean spirited, sadistic fashion. 97
It is noteworthy that Mr. Kaczynski complained bitterly about his mother whom he described as emotionally distant. Given that his father committed suicide, and his brother spent almost a year living in a hole in the ground which he covered with a tarp, 97 it is possible that Ted Kaczynski may have been genetically at risk; which is why even a brief separation may have wrought such catastrophic consequences.
The amygdala, septal nuclei, cingulate gyrus, and hippocampus subserve all aspects of social and emotional functioning including the capacity to establish, remember, and maintain emotional attachments. These limbic system nuclei are also exceedingly plastic, "experience-expectant," and require considerable emotional, social, and maternal stimulation in order to develop normally. If denied sufficient input limbic system neurons involved in perceiving social emotional nuances, such as conveyed by the face, through body language, and the spoken word, and those responsible for forming and remembering emotional attachments, may atrophy, develop abnormal activity, form or maintain inappropriate or random interconnections, or come to be invaded by competing neural assemblies, and in consequence function abnormally.