An analysis of the electrical activity of the mammalian olfactory system

A}I

A}IAIYSIS

OF T}IE

ELECTRICAL _ACTIVITY

0F

^THE MTAIvÍMALIAI,{ OLFACTORY SYSTEM

A

thesis

submitted

for the

degree

of

Doctor

of

Philosophy

by

PETER POLSON,

B"E.

^(Hons.)

Department

of Electrical

Engineering,

University of

^Adelaide,

Australia.

Decernber, 1971

Æ\

É% F,

^,,v¿

ê

\to""9j

è/

RTCHARD EATON

M.D.,

LL.D.

1842

-

¹⁹²⁶

British

sungeon, inaugu:ral H¡ofesson

of Physiolory a¡rd

pno-Chancel1or,

tlnivensity of

Liveqpool

; the fir"st person to

reccn¡d

the electr"ical

activity of the brai¡.

T0 MY ^\d I FE

,

^KERYN.

Chapter

TABLE OF CONTENTS

SI.'MMARY OF T}IIS TMSIS

STATEMENT

ACKNOWLEDGEMENTS

INTRODUCTION

General com¡nents

Neryous systen

structure,

Purpose

of this

research and

centrifugal

mechanisns rHE OLFACTORY _SYSTEM

General comrnents

Structure of the olfactory

system The primary receptoïs

The

olfactory

bulb The

olfactory

formation

The accessory

olfactory

formation

connections

of the bulb with tertiary olfactory

centres Connections

with the pyriform

cortex

Connections

with the anterior olfactory

nucleus Connections

within the olfactory

bulb

The granule

cells of the olfactory

bulb

SECTION

A

POTENTIALS EVOKED BY ELECTRICAL STIMULATION TYPES ATID PROPERTIES OF OLFACTORY BULB EVOKED POTENTIALS

Outline of this

chapter General comments

Methods

Experimental _animals Anaesthesia

Surgical

nethods

Stimulation

and recording techniques Results

The

three

most cornrnon

bulbar

evoked responses

Effect of

anaesthetic on

bulbar

evoked iesponses Conposite

nature of the

LOT/cortex response

Results

of other

authors

Hypothesis on

nature of

LOT/cortex ïesponse AERs obtained during

penetration of stimulating

electrode

Responses from

the rat Arti

facts

Page

I

_1-1

1-1

t-2

1-8

II

III

2-L

2-t

2-3 2-4

) -q,

2-6

2-It

2-13 2-73 2-L5 2-77 2-24

3-L

3-r

3-2 3-2 3-2 3-3 3-4 3-5 3-7 3-9 3-L2 3-12

3-t4

3- 15

3-17 3- 19

3-20

Chapter (contd)

III

IV

VI

Page

3-2\

Responses

fron the

guinea pig

lÐT/cortex

response

interactions to

double-pulse

stimulation

Threshold responses

Type

5

^(crossed

negative)

responses and properties Type

6

(rrotherrr) Tesponses

Bulbar responses

to stimulation in region of

claustrrrm

Pyriforu, cortex

response

to stinulation of ipsilateral olfactory

bulb

Discussion

THEORY I.JNDERLYING POTENTIAL DISTRIBUTION IN THE OLFACTORY BULB

Outline of this

chapter General comments

Approaches

to the

study

of extracellular potential fie

lds

Mathenatics

of field

^theory

Static

and

quasi-static fields

The

effect of tissue

capacitance

Relatíve radial resistance estinates, revisited

FIELD PLOTS OF ^OLFACTORY BULB EVOKED RESPONSES

Outline of thís

chapter General comments

Methods

Data

handling

and processing Results

Stinulating sites

Recording

sites

Exanple AER nontages

Plane 1

potential fields

Pla¡re 3

potential fields

Plane

4 results

Plane

6 results

Plane

2 results

Discussion

RADIAT POTENTIAL A},ID CURRENT SOURCE-SINK DISTRIBUTION

IN ^{THE OLFACTORY BULB}

Outline of this

chapter General comments

Methods

3-21 3-23 3-24 3-26

3-27 3-30 3-32

V

4-3 4-6 4-t5 4-t7 4-27 5-0 5-0 5-1 5-2 5-4 s-4 5-4 5-5 5.6 5-7 5-8 5-11 5-L2 5-r2 5-L7 5-2r 4-L 4-L 4-2

6-0 6-0

6-l

6-2

Ctrapter VI (contd)

VII

VIII

IX

Page

6-5 6-6

6-1.6 6- ¹⁸

6-21

7-1 7-L 7-L 7-7

8-1 8-1 8-1 8-7 8- ¹⁰ 8-22 Results

Guinea

pig

^R51

Guinea

pig

^R52

Rabbir R55

Discussion

DISCUSSION OF RECENTLY PUBLISHED RESULTS OF OTHER AUTHORS

Outline of this

chapter R.A. Nico1l

M.E. Westecker

SECTION

B

SPONTAÀIEOUS ATID INDUCED WAVE ACTIVITY

OLFACTORY BULB RESPONSES TO PULSATILE ODORAI{T STIMULATION

Outline of this

chapter General comments

Methods

Results

Dis cussi on

QUAI'{TITATIVE ANALYSIS OF ^OLFACTORY BULB SPONTANIEOUS

A}ID INDUCED WAVE ACTIVITY

Part A

Methods

of

^EEG

Analysis -

A Survey

Outline of Part

A

General comrnents

Scope

of

discussion

Exponenti

al

^repres entati ons

Time-varying spectra

Instantaneous power spectra

Fourier

transform

of a

time-varyíng autocomelation function

Tirne-varying power

density

spectra Tine-window approach

Frequency-window approach

Equivalence

of time -

and frequency-window approaches Spectrum representations

for non-stationary

data Complex demodulation

Instantaneous frequency, phase,

md

amplitude Measurement

of

instantaneous amplitude and phase

Usefulness

in

analysing signals Other representations

of a

signal Generalised spectrurn analysis

Summary

9A- 1

9A- 1

9^-2 9^-2 9A-4 9A-8 9A- 10

9A-Lz 9A-r.3 9A- 14 9A- 15 9A- 15

9A-18 9A-2r 9^-24 9^-27 9^-27 9A-28 9A- 31 9A-31

Chapter IX (contd)

Appendix ¹ Appendix ²

Appendix ³

Appendix ⁴

Appendix ⁵

Part B

Time Varying Spectrum Analysis Applications

Outline of Part

^B

General conments Methods

Results Discussion

CONCLUSIONS, CONJECTURES,

ND

RECOMMENDATIONS FOR FURTHER WORK

Review

Results

of Price

and Powell Generators

of bulbar potentials

Granule ce1ls

Active

versus passive nechanisns

in

granule

cells

Conduction

with

decrement

Unit

studies

Averaged evoked responses

Mitra1 cells

Gerunules

Reconnendations

for further

work

Electrodes, stinulation,

^{and recording}

Stereotaxic

techniques

Instrumentation Atlases

Data

collection,

conversion,

md

processing

(A) electrically

evoked responses

(B)

spontaneous and induced

activity

Input of

experimental data

to the

CDC 6400

Conversion

of

^Mnemetron CAT

digital

output

to

equivalent

voltage

input

Field plots by

conputer technique Boundary cons iderations

Programs TTSURFACETT and ^TTSURFPL|T

BIBLIOGRAPHY

Page

98- ¹ 9B-1 98- ¹ 98- 8

9B-9 98-18

X

10- 1

10- 1

L0-4 10-

I

10- 10

r0-12

10- 13 10- ^1_6

L0-t7 L0-2t L0-23 r0-24

A1- ¹

A2-t

^2-1

^2-S A3- ¹ A3- ¹ A3-6 A3- 10

A4-1

A5-1 A5-9

B-1

SUMMARY

chapter

r

introduces

the topics of

nervous systen

structure

and

function

a¡rd

traces the

development

of

understanding

of centrifugal

mechanisms. _The purpose

of the

present research

is

then described.

In

Chapter

rr, a detailed

_review

of

knowredge

of olfactory

system

stTucture,

_{based on}

recent publications, is

given.

.lfactory

system

electrical activity

may

be

convenientry subdivided

into

two broad

categories. section A,

comprising chapters

rlr to vrr, is

concerned

with electrical potentials

_evoked

in

the

olfactory bulb of the rabbit, rat,

guinea

pig,

and

cat

by

stimulation of

more

centrar sites of the brain. section B,

conprising _chapters

vlrr

and

rx, is

concerned

nainry with olfactory

_burb spontaneous and induced wave

activity in the

cat.

systeuratic

crassification

_and

description of properties of various bulbar

evoked responses

is

attempted

in

chapter

Irr.

several

novel findings

concerning

the nature

and

properties of different

responses

are

elucidated.

The theory underlying

potential distribution in

nen¡ous tissue

is investigated in

chapter

IV to provide a theoretical basis for

sub- sequent source-sink

distribution

_studies.

Digitar

conputer

plots

reproduced

in

chapter

v

show

the

three_

dimensional

distribution of potential fields

and

cu'rent

sources _and

sinks in the olfactory bulb resulting

from

stinulation of

prepyriform and perianygdaloid regions

of the pyriform cortex.

The

high

degree

of

hemispherical _syrunetry

of the fields

found

in the rostral half of

the

bulb forns the basis of the

methodology

of

chapter

vI,

where

the fine distribution of the fields is

investigated.

rn

chapter

vr, graphical differentiation

techniques are

applied to radial potential distribution

curves

to yield

measures

of the current

source-sink

distributions for the Lateral Olfactory

Tract a¡rd

Anterior

commissure types

of response.

These

distributions

are then

related to

known

bulbar

norphology.

Chapter

VII

contains

a detailed

discussion

of recently-

pubrished

results of other authors. This is

necess ary

to

emphasize some

of the original contributions of the

present study and

to

^resolve

disagreements between

their results

and those

of this thesis.

An examination

of

spontaneous and induced wave

activity in

the unanaesthetised

cat is

described

in

Chapter

VIII.

The

similarity of individual

responses under

relatively

constant

conditions is

noted and

the

controversy over whether induced wave

activity is of central

or

peripheral origin, or both, is

discussed.

A survey

of releva¡rt

methods

of signal

representation which might

be

applied

to a quantitative analysis of bulbar

spontaneous and

induced wave

activity is

contained

in

chapter

IX, part A. of all

the

possible

ways

of

representing

a signalts distribution in time

^and

frequency,

the

tirne-varying spectrum

is

probably

the

most

useful

and

easiest to

comprehend.

This

nethod

is applied in Part

B

of

Chapter IX

to earlier

records

of

Chapter

VIII.

^One

result of this application

demonstrates

that 'rflaresrt in the

induced waves

are

apparently due to

a

'rbeatingtt

effect

^between two

distinct

generator peaks

in the

spectrum

at

approxinately 40 Hz.

Chapter X provides conclusions, conjectures on puzzlíng asPects

of current olfactory

systen research, hypotheses based on over-

all results of this thesis,

and recornmendations

for further

work.

Five

appendices

are

included

to

describe

details of

elec-

trical stinulation

and

recording, stereotaxic

techniques, data

collection,

conversion and processing, and

the

use

of digital

conputer techniques

to auto¡natically

^generate

field plots.

DECLARATION

I

declare

that this thesis is a

^record

of original

^work

and contains no

naterial

which has been accepted

for the

award

of

any

other

degree

or

diplorna

in

any

University.

To

the best of

^my

knowledge a¡rd

belief, the thesis

contains no

material

previously published

or written by

another person, except when due reference

is

made

in the text of the thesis.

P.

Polson Decenber 1971

ACKNOWLEDGE}IENTS

I gratefully

acknowledge

the

assistance, encouragement, guidance, and apparently

unlimited

patience afforded me

in all

aspects

of this

research over an extended

period of

time

by

my tvüo supervisors,

Dr D. I. B. Kerr

and

Dr B. R.

Davis.

Dr Barbara

J.

Dennis

kindly

taught ne

the basic

experinental techniques and procedures, and

I

am

also gratefur for her

assistance

with the preparation of cats

used

in this

study.

For nany valued

discussions,

and assistance

with the

prepar-

ation of

some

of the

diagrams contained

in this thesis, I

thank rny

friends

and colleagues, Dr

R.

G.

B.

Morrison and Dr

P. R.

Wilson.

Technical assistance has been competently given

in

the

construction of

hardware

by K. Pelz

a¡d

H. A. HuI1,

and

in the

prepar-

ation of histological slides

by

l{isses L.

G.

Fitzpatrick

and

C. A.

Ross,

to all of

whom

I

an indebted.

The photograph

of

Richard Caton used

in the

Frontispiece was rnade frorn a negative

kindly

provided

by the University Llbrary,

Liverpool.

This

research was

carried out with the financial

assistance

of a

Comnonwealth Postgraduate Award (1965-1968),

æd

subsequently a

University

Research Grant from

the University of

Adelaide (January- Septenber 1969, September-December 1970) .

Finally,

^ìrìy

greatest

debt

of gratitude is

owed

to

ny

wife.