such as "Introduction", "Conclusion"..etc
A detailed quantitative examination of fusiform cell physiology and anatomy was made in this study. The following findingswill be discussed. 1) The basal dendrite in the gerbil is shorterthan in the cat. 2) The gerbil DCN appears to lack the high-frequencyspecialization of the cat DCN. 3) High spontaneous firing ratesare correlated with basal dendrites having both rostrally andcaudally directed branches, while low spontaneous rates are correlatedwith basal dendrites having only caudally directed branches. 4)The inhibition reflected in the slope of the regularity histogramis related to the orientation of the apical arbor. 5) Noise responsestrength appears to be systemically organized within an isofrequencysheet.
Consideration of the basal arbor total length
The basal dendrites in the gerbil have about 70% the total length that they do in the cat and thus may be electrotonicallymore compact. The equivalent cylinder model for a dendritic arborhas a characteristic electrotonic length, which is proportionalto the ratio of the physical length of the cylinder to the squareroot of its diameter (Rall 1977). Consider a hypothetical catfusiform cell that has three primary basal dendrites giving riseto identical branching structures. One possibility is that the"gerbil" fusiform cell retains all three branches, but each branchis shortened by a third. The equivalent cylinder for such a cellwould be physically shorter than its counterpart in the cat, buthave the same diameter and hence a shorter electrotonic length.A gerbil fusiform cell could also be produced by removing oneof the three hypothetical branches, giving the observed one-thirdreduction in total length. The equivalent cylinder would havethe same physical length as the cat fusiform cell, but its diameterwould be smaller, resulting in a longer electrotoniclength.
Which case best represents the actual situation? Blackstad et al. did not report branch order statistics for the cat, so itis not possible to make a comparison in this regard. But, as shownin Table 2, the height of the basal arbor is about one-thirdsmaller in the gerbil than in the cat. This would seem to rejectthe second scenario above, since the pruning of one branch wouldnot affect the size of the remaining branches and hence the arborheight should remain about the same. This leaves the first scenarioas the most viable and suggests that the effect of dendritic shorteningin the gerbil is to make the basal arbor electrotonically morecompact than in thecat.
Assuming that inputs from the auditory nerve are distributed toward the distal ends of the basal dendrites (Smith and Rhode1985), a possible effect of this electrotonic shortening wouldbe to decrease the attenuation of excitatory synaptic potentials.To the extent that inhibitory inputs are received at more proximallocations (Berrebi and Mugnaini 1991; Saint-Marie et al. 1991),they are relatively unaffected by the overall length of the dendrite.Hence, an electrotonically more compact basal dendrite might preferentiallyenhance excitatory drive relative to inhibition. Indeed, previousresults suggest that the proportion of DCN units having type IVunit properties is smaller in the gerbil than in the cat (11%vs. 32-45%) and the proportion of type III units is larger (62%vs. 23%) (Davis et al. 1996). Ding et al. (1999) reported on 13 labeled fusiform cells from the decerebrate gerbil, none of whichhad classic type IV unit response properties. Interestingly, thetype IV unit incidence in rabbit (23%) and chinchilla (25%) appearsto follow the same size-related trend (Davis et al. 1996; Huiand Disterhoft 1980; Kaltenbach and Saunders 1987).
This species-related difference in unit incidence was considered by Davis and Voigt (1996) using a point neuron model. Theirhypothesis was that a weakened contingent of type II unit inhibitiononto DCN projection neurons was responsible for the lack of typeIV units found in the gerbil relative to the cat. They showedthat a 40-50% reduction in the number of type II unit inputs wassufficient to turn a model type IV unit into a type IV-T or typeIII unit. A hypothesis based on the present finding in regardto basal dendrite length, in contrast, suggests that the balanceis shifted toward excitation by an enhancement of the excitatoryinputs, rather than by a reduction of the inhibitory inputs. Theseissues might effectively be explored using a compartmental modelof a fusiformcell.
Tonotopic organization of the gerbil DCN
The qualitative picture of tonotopy presented in Fig. 2 agrees well with the description of frequency organization in gerbilDCN obtained using measurements of 2-deoxyglucose uptake (Ryanet al. 1982). On a more quantitative basis, the fusiform cellBFs were plotted in Fig. 3 as a function of the cell positionalong the tonotopic axis. The data plotted in this manner correspondwell with the cochlea place-frequency map determined by Müller(1996) in the Mongolian gerbil (Fig. 3). Such quantitative correspondencebetween frequency representation in the cochlea and tonotopicorganization in central auditory structures is frequently observed(Müller 1990).
A notable exception is the cat DCN, whose representation of the 8- to 30-kHz range is disproportionately larger than the representationof the same frequency range in the cochlea (Spirou et al. 1993).The head-related transfer function (HRTF) in the cat containsspectral notches that may serve as cues for determining soundsource elevation (Rice et al. 1992). These notches fall in the8- to 30-kHz range, suggesting that the enhanced representationof these frequencies in the cat DCN is a functional specializationrelated to coding those particular spectral features (Spirou etal. 1993).
The place-frequency analysis shown in Fig. 3 is limited to the extent that it is a one-dimensional description of the tonotopy;it does not consider variations in cell density or the possibilityof a two-dimensional frequency gradient. The comparison with thecat data of Spirou et al. (1993) is appropriate insofar as thecat data are also based on a one-dimensional frequency axis. Thatstudy, however, was based on BF estimates made at finely spacedlocations from a large number of electrode tracks. Furthermore,Spirou et al. (1993) accounted for variations in fusiform celldensity when drawing conclusions about BF representation in theDCN.
The present data therefore should be regarded as preliminary but appear to underscore the fact that the tonotopy of the gerbilDCN (and cochlea) is largely devoted to a lower frequency range.Frequencies below 10 kHz occupy about 60% of the length of bothstructures, and no specialized frequency representation in thegerbil DCN is apparent. It is currently unknown whether or notthe gerbil HRTF contains spectral elevation cues similar to thoseidentified in the cat HRTF. Measurements of the HRTF in gerbiland a more detailed examination of frequency representation inthe DCN are essential to a comparative evaluation of DCN functionin the twospecies.
Spontaneous rate
The results indicate that the disposition of the basal dendrites is correlated with spontaneous rate for the fusiform cellswith best frequencies less than 2 kHz. The basal dendrites oflow SR cells are directed away from the soma only in the caudaldirection, while the high SR cells have basal dendrite branchesextending both rostrally and caudally. The basal arbors of thelow SR units, relative to those of the high SR units, have morecaudally located centroids. It is important to note that thisobservation is based on relative comparisons of basal arbor structureamong cells having similar orientations. No absolute metric wasfound to allow for a global quantification of the relationshipbetween SR and basal dendrite position. It was thus necessaryto limit consideration to this BF range because of the generalshift in long axis orientation with rostral-caudal position (andhence BF) and because there were not sufficient numbers in anyother frequency band for cell-to-cell comparisons to bemade.
It is not immediately clear how the orientation of the basal dendrites may influence spontaneous activity. Liberman (1993)suggested that auditory nerve inputs to the cat DCN may be segregatedbased on spontaneous rate, with the high SR fibers terminatingdeeper in the nucleus than the low SR fibers. This appears tobe inconsistent with our results, since the rostrally directedbasal dendrites of the high SR fusiform cells tend to be moreshallow in depth than the caudally directed branches common toboth SRgroups.
Another possibility is that the rostrally directed branches access some other set of inputs that modulate spontaneous activity.It also may be that the orientation characteristic of the highSR cells has electrotonic consequences that emphasize excitatoryinputs over inhibitory inputs. Regardless of the mechanism, theresults suggest that the distribution of fusiform cell spontaneousactivities is not entirely due tohappenstance.
It is difficult to say what functional consequences may arise from having a subset of the fusiform cell population preferentiallyreceive low SR input. It has been suggested that low SR auditorynerve fibers are recruited to improve intensity discriminationat high sound levels or are useful for signal in noise problems(Viemeister 1983). Extending such interpretations to the DCN isproblematic, because they are based on the fact that low SR ANfibers typically have high acoustic thresholds (Liberman 1978),a trend not generally characteristic of DCN units. It has beenshown that low SR AN fibers better synchronize to AM tones (Jorisand Yin 1992), but there remains disagreement over the generalsuitability of DCN projection neurons for encoding such stimuli(Joris and Smith 1998).
Shape of regularity histogram
For the fusiform cells in the 0- to 2-kHz band, a correlation was observed between the orientation of the apical dendriticarbor, quantified by the rotation, apical, about the long axisyielding the narrowest projection of the arbor, and the shapeof the regularity histogram, as quantified by the slope, m1 (Fig.7). The slope values m1 and m2 are obtained by simultaneouslyfitting two lines to the interspike interval plot after omittingthe first bin. For the data of this study, the value of m1 appearsto be a more useful measure of inhibition than the monotonicityof the BF rate-level curve, because the m1 values are more evenlydistributed over a wider interval. A positive value of m1 reflectsa rate trend similar to the underlying excitatory drive from auditorynerve fibers and hence suggests relatively weak inhibitory input.Negative values are taken as an indication of a relatively strongerinhibitorycontribution.
One interpretation of this result is that the apical dendrite orientation determines the cross-sectional area of the arborperpendicular to the trajectory of the parallel fibers and henceaffects the pattern of activity in the apical arbor. For example,those presenting a narrow face to the parallel fiber network maybe more strongly influenced by inhibitory inputs from the cartwheelcell population. Although cartwheel cells are known to be acousticallyresponsive, their activity is relatively weak and of high threshold(Ding et al. 1999; Parham and Kim 1995) and would not be expectedto account for the relatively strong inhibition represented bynegative values of m1.
A second possibility is that since the neurons represented in Fig. 7 come from the ventrolateral third of the nucleus, thechange in apical arbor orientation may result from curvature ofthe strial axis in this region (Blackstad et al. 1984). In thiscase, the variations in orientation and in slope m1 may, in fact,be functions of position. That no such dependence was apparentin our position data may indicate limitations in the accuracyof mapping position across different tissuesamples.
Possible significance of physiology-morphology correlations
Figures 5-7 demonstrate that certain morphological features are correlated with specific physiological properties. The geometriesof the apical and basal arbors influence input resistance andspontaneous activity, respectively, while some aspect of cellorientation apparently contributes to the inhibition measuredin the regularity histogram. It is thus possible that fusiformcells along the isofrequency axis have graded physiological properties,and hence different signal processing characteristics. In thisway, the fusiform cell population might be capable of performingdifferent operations on the same set ofinputs.
A chance example from the present study illustrates that significant morphological differences may indeed exist between nearbycells. Figure 9 is a sagittal view of two fusiform cells, labeledin a single electrode track, their cell bodies separated by lessthan 10 µm. They were located in the caudal DCN, and hence, asdescribed earlier, their long axes have a rostral-to-caudal orientation.The apical arbor of the black-colored neuron is sparser than thatof the gray-colored neuron. Furthermore, the two basal arborsdo not overlap completely, but follow slightly different trajectories.The results of Fig. 9 support the notion that neighboring fusiformcells might have markedly different morphologies.
Organization of sensitivity to broadband noise
The notion that the DCN contains a functional axis orthogonal to the frequency axis is suggested by anatomical features. First,there is the network of parallel fibers oriented perpendicularto the underlying auditory nerve fibers. If systematic variationsin activity within the parallel fiber network contribute to thevariations in fusiform cell physiology, then fusiform cell propertiesmight vary in a spatially dependent manner. Another anatomicalsubstrate for a second axis in the DCN is a progressive decreasein the number of vertical cells in the dorsomedial direction withinthe coronal plane (Lorente de Nó 1981). Since vertical cellspresumably inhibit fusiform cells, the magnitude of inhibitoryresponse features (tone slope, interspike interval slope, etc.)should also decrease in the dorsomedialdirection.
The results show that the relative noise index is negatively correlated with position in the ventrolateral to dorsomedialdirection (Fig. 8A). In other words, fusiform cell responses tonoise tend to become weaker in the same general direction in whichLorente de Nó (1981) reported the vertical cell layer becomingthinner. A decrease in the number of vertical cells, however,represents a loss of inhibition and so cannot account for thediminishing noise responses. The noise sensitivity of DCN principalcells is thought to be shaped by a source of wideband inhibition,possibly originating in the PVCN (Nelken and Young 1994). Theobserved noise responses in the current study might be accountedfor by an increasing contribution of this inhibitory source inthe dorsomedialdirection.
Earlier studies have identified two inhibitory components to the response maps of type IV units, as schematized in Fig. 10.The first arises from a band of type II units, centered belowthe BF of the type IV unit (Voigt and Young 1990), while the secondcomponent, wideband inhibition, possibly arises from the PVCNand is centered above the type IV unit BF (Nelken and Young 1994;Spirou and Young 1991). This organization might be consistentwith wideband inhibitory input strengthening in the dorsomedialdirection, as suggested by the present results, and the verticalcell layer thinning in the same direction, as described by Lorentede Nó. If, for example, each type IV unit receives input froma band of type II units (presumably vertical cells) centered spatiallyon BF, then the resulting inhibitory band would have a lower BFbecause the vertical cells are more dense in that direction. Similarly,if the wideband inhibition is stronger in the dorsomedial direction,inhibition from a band spatially centered on BF will itself havea higher BF. The idea that these two inhibitory sources mighttrade for one another across the width of the DCN is consistentwith data presented by Nelken and Young (1994). Their Fig. 8Bsuggests that the influence of inhibition by type II units, asmeasured by the maximum driven BF rate, is negatively correlatedwith the influence of wideband inhibition, as measured by theminimum inhibitory notch width.
Conclusion
This report has described differences between cats and gerbils in the anatomical properties of DCN fusiform cells and in theirtonotopic arrangement. The report also described systematic distributionsof functional properties within the fusiform cell population.How such variations contribute to DCN function is yet to beunderstood.
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