The right way, the wrong way, and the army way: A dendritic parable

We suggest that neither selectionism nor constructivism alone are responsible for learning-based changes in the brain. On the basis of quantitative structural studies of human brain tissue it has been possible to find evidence of both increase and decrease in tissue mass at synaptic and dendritic levels. It would appear that both processes are involved in the course of learning-dependent changes. The neurosciences have seen more than their share of impassioned conceptual dualities. Reticularism versus neuronism and “soup versus spark” synaptic transmission dynamics are two among many that come to mind. It is interesting to recall that neural reality was finally determined to encompass both poles of each duality. Neurons were indubitably separate entities but in the case of gap junctions, virtually continuous through the agency of connexions establishing structural continuity for ion flow. Neurons clearly communicate through the agency of neurotransmitter release but “electrical” transmission remains a reality at gap junctions. I would suggest that we may be dealing with another impassioned duality in the matter of “selectionism versus constructivism.” Quartz & Sejnowski (Q&S) have presented powerful evidence supporting environmentally engendered dendritic and axonal growth. Ideationally implicit in the work of Ramon y Cajal (1952) and further explored at the conceptual level by Hebb (1949), the conjectures became reality at the chemical level in the studies of Krech et al. (1960) and, at the structural level, in the extended series of studies by Diamond and her collaborators (1964; 1975; 1988) and in a number of other findings. Our own quantitative histological studies of human cerebral cortex argued strongly for causal links between computational complexity and structural complexity (Scheibel et al. 1990). Thus dendritic elaboration in the primary sensory cortical representational area for hand and fingers was significantly greater than that in the adjacent area for trunk representation. Furthermore, there were “suggestive associations between the complexity of dendrite systems of the handfinger zone of the primary receptive area and the nature of the work with which the individual had been associated during his/her working life” (Scheibel et al. 1990, p. 85). Furthermore the conjoint development of language facility and waxing dendrite elaboration in Broca’s area of the language-dominant hemisphere (Simmonds & Scheibel 1989) provided correlative if not causal relations between escalating cognitive demands and expanding neuropil. Arguments can also be advanced for selectionism, however. In several series of electron microscope studies performed on rodents, measurable and significant decreases in the number of synaptic terminals in cortical axo-spino-dendritic synapses accompanied exposure to enriched environments (e.g., Mollgard et al. 1971). Individual synaptic terminals showed significant increase in the length of the postsynaptic thickening, thereby suggesting the presence of fewer, but larger and more effective synapses in environmentally enriched animals. Further analysis of these changes indicated that the effects of enriched environmental input as expressed in loss of synaptic terminals and enlargement of the remainder actually increased with age (Diamond et al. 1975). And the enriched rats were quicker maze-learners than their nonenriched mates (Diamond 1988)! Assuming that a complex interweaving of dendritic/synaptic gain and loss are involved in the maturation-learning process, a third mechanism seems intertwined with these two, adding to the richness and subtlety of the process. Quantitative comparisons of dendritic tissue in Broca’s area of left and right hemispheres revealed an unexpected result (Scheibel et al. 1985). There was no significant difference between the total dendritic length of neurons on either side. What did differ was the amount of dendritic length ‘invested’ in various portions of each dendritic tree. On the right, the non-language-dominant side, most of the dendrite length was involved in the first three orders of dendrite branching. On the language-dominant side, a much greater proportion of dendrite length was devoted to the outer branches (fourth, fifth, sixth order dendrite branches, etc.). Note that the inner, lower order branches developed earlier in the developmental history of the individual, while the outer branching segments developed later. Thus both temporal patterns of development and position on the dendrite tree were significant parameters in CNS growth and maturation. Note also, that successive additions to the periphery of the dendrite ensemble should (at least theoretically) not affect the more central parts of the dendrite system where synaptic patterns had presumably already been established. However, more than a tidy “add-on” effect was noted here. Our data (Simmonds & Scheibel 1989) strongly suggested that along with the pattern of use-dependent centrifugal growth there was also a related (and presumably use-dependent) partial resorption of lower order branches more centrally located within the dendrite ensemble. Simultaneous involvement of cortical dendritic tissue gain and loss during the maturation-learning process argues for the inextricable combination of constructivist and selectionist processes. Neural constraints on cognitive modularity?