Brain architecture and social complexity in modern and ancient birds

Vertebrate brains vary tremendously in size, but differences in form are more subtle. To bring out functional contrasts that are independent of absolute size, we have normalized brain component sizes to whole brain volume. The set of such volume fractions is the cerebrotype of a species. Using this approach in mammals we previously identified specific associations between cerebrotype and behavioral specializations. Among primates, cerebrotypes are linked principally to enlargement of the cerebral cortex and are associated with increases in the complexity of social structure. Here we extend this analysis to include a second major vertebrate group, the birds. In birds the telencephalic volume fraction is strongly correlated with social complexity. This correlation accounts for almost half of the observed variation in telencephalic size, more than any other behavioral specialization examined, including the ability to learn song. A prominent exception to this pattern is owls, which are not social but still have very large forebrains. Interpolating the overall correlation for Archaeopteryx, an ancient bird, suggests that its social complexity was likely to have been on a par with modern domesticated chickens. Telencephalic volume fraction outperforms residuals-based measures of brain size at separating birds by social structure. Telencephalic volume fraction may be an anatomical substrate for social complexity, and perhaps cognitive ability, that can be generalized across a range of vertebrate brains, including dinosaurs.     

Maternal effects and the evolution of brain size in birds: overlooked developmental constraints

A central dogma for the evolution of brain size posits that the maintenance of large brains incurs developmental costs, because they need prolonged periods to grow during the early ontogeny. Such constraints are supported by the interspecific relationship between ontological differences and relative brain size in birds and mammals. Given that mothers can strongly influence the development of the offspring via maternal effects that potentially involve substances essential for growing brains, we argue that such effects may represent an important but overlooked component of developmental constraints on brain size. To demonstrate the importance of maternal effect on the evolution of brains, we investigated the interspecific relationship between relative brain size and maternal effects, as reflected by yolk testosterone, carotenoids, and vitamins A and E in a phylogenetic study of birds. Females of species with relatively large brains invested more in eggs in terms of testosterone and vitamin E than females of species with small brains. The effects of carotenoid and vitamin A levels on the evolution of relative brain size were weaker and non-significant. The association between relative brain size and yolk testosterone was curvilinear, suggesting that very high testosterone levels can be suppressive. However, at least in moderate physiological ranges, the positive relationship between components of maternal effects and relative brain size may imply one aspect of developmental costs of large brains. The relationship between vitamin E and relative brain size was weakened when we controlled for developmental mode, and thus the effect of this antioxidant may be indirect. Testosterone-enhanced neurogenesis and vitamin E-mediated defence against oxidative stress may have key functions when the brain of the embryo develops, with evolutionary consequences for relative brain size.     

Developmental origins of mosaic brain evolution: Morphometric analysis of the developing zebra finch brain

In adult zebra finches (Taeniopygia guttata), the telencephalon occupies 64% of the entire brain. This fraction is similar to what is seen in parrots, but many other birds possess a significantly smaller telencephalon. The aim of the present study was to determine the developmental time course and cellular basis of telencephalic enlargement in zebra finches, and then to compare these findings with what is known about telencephalic enlargement in other birds. To this end we estimated the volumes of all major brain regions from serial sections in embryonic and post‐hatching zebra finches. We also labeled proliferating cells with antibodies against proliferating cell nuclear antigen and phosphorylated histone H3. An important finding to emerge from this work is that the telencephalon of zebra finches at hatching contains a thick proliferative subventricular zone (SVZ) that extends from the subpallium into the dorsal pallium. The data also show that the onset and offset of telencephalic neurogenesis are both delayed in zebra finches relative to quail (Galliformes). This delay in neurogenesis, in conjunction with the expanded SVZ, probably accounts for most of the telencephalic enlargement in passerines such as the zebra finch. In addition, passerines enlarged their telencephalon by decreasing the proportional size of their midbrain tectum. Because the presumptive tectum is proportionally smaller in zebra finches than quail before neurogenesis begins, this difference in tectum size cannot be due to evolutionary alterations in neurogenesis timing. Collectively these findings indicate that several different developmental mechanisms underlie the evolution of a large telencephalon in passerines. J. Comp. Neurol. 514:203–213, 2009. © 2009 Wiley‐Liss, Inc.     

Anatomical organization of the visual dorsal ventricular ridge in the chick (Gallus gallus): Layers and columns in the avian pallium

The dorsal ventricular ridge (DVR) is one of the main components of the sauropsid pallium. In birds, the DVR is formed by an inner region, the nidopallium, and a more dorsal region, the mesopallium. The nidopallium contains discrete areas that receive auditory, visual, and multisensory collothalamic projections. These nidopallial nuclei are known to sustain reciprocal, short‐range projections with their overlying mesopallial areas. Recent findings on the anatomical organization of the auditory DVR have shown that these short‐range projections have a columnar organization that closely resembles that of the mammalian neocortex. However, it is unclear whether this columnar organization generalizes to other areas within the DVR. Here we examine in detail the organization of the visual DVR, performing small, circumscribed deposits of neuronal tracers as well as intracellular fillings in brain slices. We show that the visual DVR is organized in three main laminae, the thalamorecipient nucleus entopallium; a dorsally adjacent nidopallial lamina, the intermediate nidopallium; and a contiguous portion of the ventral mesopallium, the mesopallium ventrale. As in the case of the auditory DVR, we found a highly topographically organized system of reciprocal interconnections among these layers, which was formed by dorsoventrally oriented, discrete columnar bundles of axons. We conclude that the columnar organization previously demonstrated in the auditory DVR is not a unique feature but a general characteristic of the avian sensory pallium. We discuss these results in the context of a comparison between sauropsid and mammalian pallial organization. J. Comp. Neurol. 523:2618–2636, 2015. © 2015 Wiley Periodicals, Inc.     

Encephalization in hummingbirds (Trochilidae)

The brain mass in 23 hummingbird species was compared to that in galliform birds taking body mass into consideration. Hummingbird brain masses were determined by endocranial volumes, and their body masses were calculated from skeletal measurements. Galliform data were taken from a recent publication. Hummingbirds have brains that are approximately 2.5 times larger than those of galliform birds. Such encephalization may be due to (1) an enlargement of the telencephalon, or (2) an enlargement of functionally well-defined extratelencephalic brain parts. Based on the extremely specialized feeding behavior of the nectarivorous hummingbirds and the neurological demands associated with sucking nectar during hovering, the second hypothesis is better supported, but further studies are needed.     

Hippocampal volume does not change seasonally in a non food-storing songbird.

Seasonal differences in hippocampal morphology have been reported in food-storing birds. Non food-storing species have not been investigated however. It is therefore unclear whether seasonal changes in the hippocampus are specifically related to food-storing or reflect a more general seasonal mechanism that occurs in both food-storing and non food-storing birds alike. We determined the volumes of the hippocampal formation and remaining telencephalon in the non-storing male song sparrow (Melospiza melodies morphna) in two experiments comparing birds collected in the spring and fall of 1992-94 (Experiment 1) and 1997 (Experiment 2). Although pronounced seasonal changes in song control nuclei such as the HVC and RA were previously reported for the same brains used in Experiment 1, we found that hippocampal volume did not change with season in either Experiment 1 or 2 for these song sparrow brains. These results suggest that seasonal changes in the hippocampus do not occur in this non food-storing species and may be specific to food-storing birds.     

Individual variability in cortical organization: its relationship to brain laterality and implications to function

The human brain and the brains of most mammals studied for this purpose demonstrate hemispheric asymmetry of gross anatomical landmarks and/or architectonic cortical subdivisions. The magnitude as well as the direction of these cortical asymmetries vary among individuals, and in some species there exist significant population directional biases. The magnitude, if not the direction, of cortical asymmetry is found to predict for relative numbers of neurons comprising a given pair of hemispheric architectonic homologues such that the more asymmetric the region is, the smaller the number of neurons. Similarly, the more asymmetric a region is, the smaller the density of interhemispheric connections and (probably) the greater the density of intrahemispheric connections. Developmentally, the decrease in the number of neurons characterizing the more asymmetrical regions appears to reflect mainly increased unilateral ontogenetic cell loss, and diminished callosal connectivity might signify increased developmental axonal pruning. These relationships between cell numbers, callosal connections, and presumed intrahemispheric relationships can be entertained to explain variability in anatomo-clinical correlations for language function and aphasia between left- and right-handers and men and women.     

Subcortical brain volumes relate to neurocognition in schizophrenia and bipolar disorder and healthy controls

Background

Similar patterns of subcortical brain abnormalities and neurocognitive dysfunction have been demonstrated in schizophrenia and bipolar disorder, with more extensive findings in schizophrenia. It is unknown whether relationships between subcortical volumes and neurocognitive performance are similar or different between schizophrenia and bipolar disorder.

Methods

MRI scans and neuropsychological test performance were obtained from 117 schizophrenia or 121 bipolar spectrum disorder patients and 192 healthy control subjects. Using the FreeSurfer software, volumes of 18 selected subcortical structures were automatically segmented and analyzed for relationships with results from 7 neurocognitive tests.

Results

In schizophrenia, larger left ventricular volumes were related to poorer motor speed, and bilateral putamen volumes were related to poorer verbal learning, executive functioning and working memory performance. In bipolar disorder, larger left ventricular volumes were related to poorer motor speed and executive functioning. The relationship between left putamen volume and working memory was specific to schizophrenia. The relationships between left inferior lateral ventricles and motor speed and between right putamen volumes and executive functioning were similar in schizophrenia and bipolar disorder, and different from healthy controls. The results remained significant after corrections for use of antipsychotic medication. Significant structure-function relationships were also found when all subjects were combined into one group.

Conclusion

The present findings suggest that there are differences as well as similarities in subcortical structure/function relationships between patients with schizophrenia or bipolar disorder and healthy individuals. The observed differences further suggest that ventricular and putamen volume sizes may reflect severity of cognitive dysfunction in these disorders.     

Interspecific allometry of the brain and brain regions in parrots (psittaciformes): comparisons with other birds and primates

Despite significant progress in understanding the evolution of the mammalian brain, relatively little is known of the patterns of evolutionary change in the avian brain. In particular, statements regarding which avian taxa have relatively larger brains and brain regions are based on small sample sizes and statistical analyses are generally lacking. We tested whether psittaciforms (parrots, cockatoos and lorikeets) have larger brains and forebrains than other birds using both conventional and phylogenetically based methods. In addition, we compared the psittaciforms to primates to determine if cognitive similarities between the two groups were reflected by similarities in brain and telencephalic volumes. Overall, psittaciforms have relatively larger brains and telencephala than most other non-passerine orders. No significant difference in relative brain or telencephalic volume was detected between psittaciforms and passerines. Comparisons of other brain region sizes between psittaciforms and other birds, however, exhibited conflicting results depending upon whether body mass or a brain volume remainder (total brain volume - brain region volume) was used as a scaling variable. When compared to primates, psittaciforms possessed similar relative brain and telencephalic volumes. The only exception to this was that in some analyses psittaciforms had significantly larger telencephala than primates of similar brain volume. The results therefore provide empirical evidence for previous claims that psittaciforms possess relatively large brains and telencephala. Despite the variability in the results, it is clear that psittaciforms tend to possess large brains and telencephala relative to non-passerines and are similar to primates in this regard. Although it could be suggested that this reflects the advanced cognitive abilities of psittaciforms, similar studies performed in corvids and other avian taxa will be required before this claim can be made with any certainty.     

Avian and mammalian "prefrontal cortices": limited degrees of freedom in the evolution of the neural mechanisms of goal-state maintenance

Is it possible to produce the same cognitive function with different brain organizations? This question is approached for working memory, a cognitive entity that is equally organized in birds and mammals. The critical forebrain structure for working memory is the nidopallium caudolaterale (NCL) in birds and the prefrontal cortex (PFC) in mammals. Although both structures share a large number of neural architectural features, they are probably not homologous but represent a remarkable case of convergent evolution. In reviewing the neuronal mechanisms for working memory in birds and mammals it becomes apparent that the similarities of NCL and PFC extend from the neuronal activation patterns during memory tasks down to the biophysical mechanisms of synaptic currents. Both in mammals and birds, dopamine acts via D1-receptors to tune preactivated neurons into sustained high-frequency patterns with which goal states can be held over time until an appropriate response can be generated. The degrees of freedom to create different neural architectures to solve the problem of 'stimulus maintenance' seem to be very small.     

Validation of a new antiserum directed towards the synthetic c-terminus of the FOS protein in avian species: immunological, physiological and behavioral evidence.

In the past 10 years, the study of the expression of immediate early genes, such as c-fos, in the brain has become a common method for the identification of brain areas involved in the regulation of specific physiological and behavioral functions. The use of this method in avian species has been limited by the paucity of suitable antibodies that cross-react with the FOS protein in birds. We describe in this paper the preparation of an antibody directed against a synthetic fragment of the protein product of the c-fos gene in chickens (Gallus domesticus). We demonstrate that this new antibody can be used in several avian species to study FOS expression induced by a variety of pharmacological, physiological and behavioral stimuli. Western blot studies indicated that this antibody recognizes a protein of the expected size (47 kDa) but also cross reacts to some extent with proteins of lower molecular weight that share sequence homology with FOS (Fos-related antigens). FOS immunocytochemistry was performed with this antibody in four species of birds in three different laboratories utilizing diverse variants of the immunocytochemical procedure. In all cases the antibody provided a reliable identification of the FOS antigen. The new antibody described here appears to be suitable for the study of FOS expression in several different avian species and situations. It is available in substantial amounts and will therefore make it possible to use FOS expression as a tool to map brain activity in birds as has now been done for several years in mammalian species.     

C-fos induction in forebrain areas of two different visual pathways during consolidation of sexual imprinting in the zebra finch (Taeniopygia guttata)

Two forebrain areas in the hyperpallium apicale and in the lateral nidopallium of isolated male zebra finches are highly active (2-deoxyglucose technique) on exposure to females for the first time, that is first courtship. These areas also demonstrate enhanced neuronal plasticity when screened with c-fos immunocytochemistry. Both are areas involved in the processing of visual information conveyed by the two major visual pathways in birds, strengthening our hypothesis that courtship in the zebra finch is a visually guided behaviour. First courtship and chased birds show enhanced c-fos induction in the hyperpallial area, which could represent neuronal activity reflecting changes in the immediate environment. The enhanced expression of fos in first courtship birds in lateral nidopallial neurons indicates imminent long-lasting changes at the synaptic level that form the substrate for imprinting, a stable form of learning in birds.     

Prevalence of cavum septum pellucidum in schizophrenia studied with MRI

OBJECTIVE: To study the prevalence of cavum septum pellucidum (CSP), a midline developmental anomaly, in patients with schizophrenia. METHODS: Three-millimeter coronal T1 weighted MRI images of 43 normal controls and 73 patients with schizophrenia were examined. The images were resampled into 1-mm slices and CSP was measured by the number of slices in which it appeared. RESULTS: Patients had significantly higher incidence of CSP (Fisher's exact test 0.042; one-sided). Eighteen (41.9%) of the controls and 44 (60.3%) of patients had a CSP, and one of 46 controls and three of 73 patients had a large CSP of six slices or more. There was no relationship between the presence or size of CSP and regional brain volumes or volumes of hippocampus-amygdala complex, caudate, superior temporal gyrus or ventricular CSF. CONCLUSION: Higher incidence of CSP may reflect a neurodevelopmental disturbance in schizophrenia.     

A comparative analysis of relative brain size in waterfowl (Anseriformes).

Variation in relative brain size was examined in 55 species of waterfowl (Anseriformes). Using both conventional statistics and phylogenetically based comparative methods, the extent of variation in relative brain size and possible relationships with mode of foraging and diet were examined. The results indicate that although brain size does vary considerably between closely related species of waterfowl, it is not reliably related to either foraging mode or diet. There are a number of possible reasons for the lack of relationships between brain size and foraging mode and diet. Firstly, subtle changes in foraging mode and diet may favor relatively large changes in brain size. Secondly, foraging mode and diet could be correlated with the expansion of an individual brain region without affecting overall brain size. Thirdly, other behavioral/ecological traits may be more important with respect to brain size evolution in waterfowl. For example, the relatively large brain of the musk duck (Biziura lobata) and altriciality of their young in comparison to other stiff-tailed ducks (Oxyura spp.) indicates that developmental rate plays a significant role in the evolution of brain size. Given the difference between our results and that reported in inter-order comparisons of brain size in birds, further research is required into other avian orders to assess how brain size and behavior might be related within orders as well as between them.     

Neurophysiological studies on atypical parkinsonian syndromes

There have been a relatively large number of experimental investigations using neurophysiological techniques in patients with atypical parkinsonian syndromes (APs), including progressive supranuclear palsy, cortico-basal syndrome and multiple system atrophy. Earlier studies focused on the startle, blink and trigemino-cervical reflexes and showed several brainstem abnormalities. Studies using transcranial magnetic stimulation have revealed a number of abnormalities in primary motor cortex and inter-hemispheric connectivity. More recent studies have highlighted the role of cerebellar dysfunction and have reported altered movement kinematics. Neurophysiological abnormalities in APs reflect degeneration or functional changes at multiple brain levels. In the majority of cases, APs share common abnormalities even though some neurophysiological changes differ among the various APs. Evidence of a correlation between neurophysiological abnormalities and clinical signs and symptoms in APs is limited. This paper provides an update on the results of experimental investigations using neurophysiological techniques in APs and also reviews similarities and differences between APs and Parkinson's disease. The potential role of neurophysiological abnormalities in the clinical context of APs is also discussed.     

Brain structural abnormalities in young children with autism spectrum disorder

OBJECTIVE: To explore the specific gross neuroanatomic substrates of this brain developmental disorder, the authors examine brain morphometric features in a large sample of carefully diagnosed 3- to 4-year-old children with autism spectrum disorder (ASD) compared with age-matched control groups of typically developing (TD) children and developmentally delayed (DD) children. METHODS: Volumes of the cerebrum, cerebellum, amygdala, and hippocampus were measured from three-dimensional coronal MR images acquired from 45 children with ASD, 26 TD children, and 14 DD children. The volumes were analyzed with respect to age, sex, volume of the cerebrum, and clinical status. RESULTS: Children with ASD were found to have significantly increased cerebral volumes compared with TD and DD children. Cerebellar volume for the ASD group was increased in comparison with the TD group, but this increase was proportional to overall increases in cerebral volume. The DD group had smaller cerebellar volumes compared with both of the other groups. Measurements of amygdalae and hippocampi in this group of young children with ASD revealed enlargement bilaterally that was proportional to overall increases in total cerebral volume. There were similar findings of cerebral enlargement for both girls and boys with ASD. For subregion analyses, structural abnormalities were observed primarily in boys, although this may reflect low statistical power issues because of the small sample (seven girls with ASD) studied. Among the ASD group, structural findings were independent of nonverbal IQ. In a subgroup of children with ASD with strictly defined autism, amygdalar enlargement was in excess of increased cerebral volume. CONCLUSIONS: These structural findings suggest abnormal brain developmental processes early in the clinical course of autism. Research currently is underway to better elucidate mechanisms underlying these structural abnormalities and their longitudinal progression.     

Resetting the Brain as Well as the Nomenclature. Reply to Szalavitz

Szalavitz’s model and mine share a good many components. Foremost among them is the conviction that addiction is a developmental trajectory, not a disease. Szalavitz is correct that we should consider controlled substance use an acceptable outcome, though I would like her to shift her terminology away from the medical mainstream. Finally, I suggest that Szalavitz's important idea of a "reset" in brain development might best be addressed by the notion of kindling.     

Prevalence of large cavum septi pellucidi and its relation to the medial temporal lobe structures in schizophrenia spectrum

Magnetic resonance imaging was used to evaluate the prevalence of the cavum septi pellucidi (CSP) in 154 schizophrenia patients, 47 schizotypal disorder patients, and 163 healthy controls. We also explored the relation of a large CSP (> or =6 mm) with medial temporal lobe structures. No significant difference was found in the prevalence of the CSP (76.0% of the schizophrenia patients, 81.6% of the controls, and 85.1% of the schizotypal patients) or the large CSP (6.5% of the schizophrenia patients, 7.4% of the controls, and 10.6% of the schizotypal patients) among the groups, but patients with a large CSP (10 schizophrenia and 5 schizotypal patients) had smaller volumes of bilateral amygdala and left posterior parahippocampal gyrus than patients without it. In the control subjects, the large CSP did not affect the volumes of the medial temporal lobe structures. These findings might reflect neurodevelopmental abnormalities in midline and associated limbic structures of the brain in schizophrenia spectrum.     

A unique ion channel clustering domain on the axon initial segment of mammalian neurons

The axon initial segment (AIS) plays a key role in initiation of action potentials and neuronal output. The plasma membrane of the AIS contains high densities of voltage‐gated ion channels required for these electrical events, and much recent work has focused on defining the mechanisms for generating and maintaining this unique neuronal plasma membrane domain. The Kv2.1 voltage‐gated potassium channel is abundantly present in large clusters on the soma and proximal dendrites of mammalian brain neurons. Kv2.1 is also a component of the ion channel repertoire at the AIS. Here we show that Kv2.1 clusters on the AIS of brain neurons across diverse mammalian species including humans define a noncanonical ion channel clustering domain deficient in Ankyrin‐G. The sites of Kv2.1 clustering on the AIS are sites where cisternal organelles, specialized intracellular calcium release membranes, come into close apposition with the plasma membrane, and are also sites of clustering of γ‐aminobutyric acid (GABA)ergic synapses. Using an antibody specific for a single Kv2.1 phosphorylation site, we find that the phosphorylation state differs between Kv2.1 clusters on the proximal and distal portions of the AIS. Together, these studies show that the sites of Kv2.1 clustering on the AIS represent specialized domains containing components of diverse neuronal signaling pathways that may contribute to local regulation of Kv2.1 function and AIS membrane excitability. J. Comp. Neurol. 522:2594–2608, 2014. © 2014 Wiley Periodicals, Inc.